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Vertebrate reproductive science and technology
REVIEW

Role of miRNAs in preimplantation embryo development and their potential as embryo selection biomarkers

Masoumeh Esmaeilivand A B , Ali Abedelahi C , Kobra Hamdi D , Laya Farzadi D , Sepide Goharitaban A C , Amir Fattahi https://orcid.org/0000-0002-5712-5336 A B D * and Behrooz Niknafs A B C *
+ Author Affiliations
- Author Affiliations

A Immunology Research Center, Tabriz University of Medical Science, Tabriz, Iran.

B Department of Reproductive Biology, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz, Iran.

C Department of Anatomical Sciences, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran.

D Women’s Reproductive Health Research Center, Tabriz University of Medical Sciences, Tabriz, Iran.


Handling Editor: Ryan Cabot

Reproduction, Fertility and Development 34(8) 589-597 https://doi.org/10.1071/RD21274
Published online: 20 April 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: MicroRNAs (miRNAs) play different roles in oocyte fertilisation, degradation of maternal transcripts, embryo development, and implantation. During in vitro fertilisation (IVF), different miRNAs are released from embryos into the spent culture media (SCM) that can potentially reflect the status of the embryo.

Aims: This study is the assessment of miRNAs, which secreted in SCM during the IVF cycles can be used as noninvasive biomarkers to predict an embryo’s ability to form a blastocyst, implant, and give live birth.

Methods: Systematic literature search was conducted to review all recent studies about miRNAs as potential non-invasive biomarkers for selecting the best embryos in the assisted reproductive technology (ART) cycle.

Key results: Studies have shown that levels of some miRNAs in the SCM have an association with the implantation potential and pregnancy outcome of the embryo.

Conclusions: Embryo-secreted miRNAs can be used as potential non-invasive biomarkers for selecting the best embryos in the ART cycle. Unfortunately, few human studies evaluated the association between ART outcomes and miRNAs in SCM.

Implications: This review can pave the way for further miRNAs transcriptomic studies on human embryo culture media and introducing a specific miRNA profile as a multivariable prediction model for embryo selection in IVF cycles.

Keywords: ART, biomarker, embryo selection, infertility, IVF, miRNAs, pregnancy, transcriptome.


References

Abu-Halima, M, Khaizaran, ZA, Ayesh, BM, Fischer, U, Khaizaran, SA, Al-Battah, F, Hammadeh, M, Keller, A, and Meese, E (2020). MicroRNAs in combined spent culture media and sperm are associated with embryo quality and pregnancy outcome. Fertility and Sterility 113, 970–980.e2.
MicroRNAs in combined spent culture media and sperm are associated with embryo quality and pregnancy outcome.Crossref | GoogleScholarGoogle Scholar | 32222254PubMed |

Amanai, M, Brahmajosyula, M, and Perry, ACF (2006). A restricted role for sperm-borne microRNAs in mammalian fertilization. Biology of Reproduction 75, 877–884.
A restricted role for sperm-borne microRNAs in mammalian fertilization.Crossref | GoogleScholarGoogle Scholar | 16943360PubMed |

Ambros, V (2004). The functions of animal microRNAs. Nature 431, 350–355.
The functions of animal microRNAs.Crossref | GoogleScholarGoogle Scholar | 15372042PubMed |

Bartel, DP (2018). Metazoan microRNAs. Cell 173, 20–51.
Metazoan microRNAs.Crossref | GoogleScholarGoogle Scholar | 29570994PubMed |

Battaglia, R, Palini, S, Vento, ME, La Ferlita, A, Lo Faro, MJ, Caroppo, E, Borzì, P, Falzone, L, Barbagallo, D, Ragusa, M, Scalia, M, D’Amato, G, Scollo, P, Musumeci, P, Purrello, M, Gravotta, E, and Di Pietro, C (2019). Identification of extracellular vesicles and characterization of miRNA expression profiles in human blastocoel fluid. Scientific Reports 9, 84.
Identification of extracellular vesicles and characterization of miRNA expression profiles in human blastocoel fluid.Crossref | GoogleScholarGoogle Scholar | 30643155PubMed |

Berg, DK, and Pfeffer, PL (2018). MicroRNA expression in bovine preimplantation embryos. Reproduction, Fertility and Development 30, 546–554.
MicroRNA expression in bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |

Berkhout, RP, Keijser, R, Repping, S, Lambalk, CB, Afink, GB, Mastenbroek, S, and Hamer, G (2020). High-quality human preimplantation embryos stimulate endometrial stromal cell migration via secretion of microRNA hsa-miR-320a. Human Reproduction 35, 1797–1807.
High-quality human preimplantation embryos stimulate endometrial stromal cell migration via secretion of microRNA hsa-miR-320a.Crossref | GoogleScholarGoogle Scholar | 32644109PubMed |

Borges, E, Setti, AS, Braga, DPAF, Geraldo, MV, Figueira, RCS, and Iaconelli, A (2016). miR-142-3p as a biomarker of blastocyst implantation failure – a pilot study. JBRA Assisted Reproduction 20, 200–205.
miR-142-3p as a biomarker of blastocyst implantation failure – a pilot study.Crossref | GoogleScholarGoogle Scholar | 28050953PubMed |

Bräutigam, C, Raggioli, A, and Winter, J (2013). The Wnt/β-catenin pathway regulates the expression of the miR-302 cluster in mouse ESCs and P19 cells. PLoS ONE 8, e75315.
The Wnt/β-catenin pathway regulates the expression of the miR-302 cluster in mouse ESCs and P19 cells.Crossref | GoogleScholarGoogle Scholar | 24040406PubMed |

Brezina, PR, Anchan, R, and Kearns, WG (2016). Preimplantation genetic testing for aneuploidy: what technology should you use and what are the differences? Journal of Assisted Reproduction and Genetics 33, 823–832.
Preimplantation genetic testing for aneuploidy: what technology should you use and what are the differences?Crossref | GoogleScholarGoogle Scholar | 27299602PubMed |

Butler, AE, Ramachandran, V, Hayat, S, Dargham, SR, Cunningham, TK, Benurwar, M, Sathyapalan, T, Najafi-Shoushtari, SH, and Atkin, SL (2019). Expression of microRNA in follicular fluid in women with and without PCOS. Scientific Reports 9, 16306.
Expression of microRNA in follicular fluid in women with and without PCOS.Crossref | GoogleScholarGoogle Scholar | 31705013PubMed |

Capalbo, A, Ubaldi, FM, Cimadomo, D, Noli, L, Khalaf, Y, Farcomeni, A, Ilic, D, and Rienzi, L (2016). MicroRNAs in spent blastocyst culture medium are derived from trophectoderm cells and can be explored for human embryo reproductive competence assessment. Fertility and Sterility 105, 225–235.e3.
MicroRNAs in spent blastocyst culture medium are derived from trophectoderm cells and can be explored for human embryo reproductive competence assessment.Crossref | GoogleScholarGoogle Scholar | 26453979PubMed |

Cheong, AWY, Pang, RTK, Liu, W-M, Kottawatta, KSA, Lee, K-F, and Yeung, WSB (2014). MicroRNA Let-7a and dicer are important in the activation and implantation of delayed implanting mouse embryos. Human Reproduction 29, 750–762.
MicroRNA Let-7a and dicer are important in the activation and implantation of delayed implanting mouse embryos.Crossref | GoogleScholarGoogle Scholar |

Cormier, S, Vandormael-Pournin, S, Babinet, C, and Cohen-Tannoudji, M (2004). Developmental expression of the Notch signaling pathway genes during mouse preimplantation development. Gene Expression Patterns 4, 713–717.
Developmental expression of the Notch signaling pathway genes during mouse preimplantation development.Crossref | GoogleScholarGoogle Scholar | 15465494PubMed |

Cuman, C, Van Sinderen, M, Gantier, MP, Rainczuk, K, Sorby, K, Rombauts, L, Osianlis, T, and Dimitriadis, E (2015). Human blastocyst secreted microRNA regulate endometrial epithelial cell adhesion. EBioMedicine 2, 1528–1535.
Human blastocyst secreted microRNA regulate endometrial epithelial cell adhesion.Crossref | GoogleScholarGoogle Scholar | 26629549PubMed |

Dorfeshan, P, Ghaffari Novin, M, Salehi, M, and Farifteh, F (2019). Expression of miR-302 in human embryo derived from in-vitro matured oocyte. International Journal of Reproductive BioMedicine 17, 405–412.
Expression of miR-302 in human embryo derived from in-vitro matured oocyte.Crossref | GoogleScholarGoogle Scholar | 31508565PubMed |

Egea, RR, Puchalt, NG, Escrivá, MM, and Varghese, AC (2014). OMICS: Current and future perspectives in reproductive medicine and technology. Journal of Human Reproductive Sciences 7, 73–92.
OMICS: Current and future perspectives in reproductive medicine and technology.Crossref | GoogleScholarGoogle Scholar | 25191020PubMed |

Fang, F, Li, Z, Yu, J, Long, Y, Zhao, Q, Ding, X, Wu, L, Shao, S, Zhang, L, and Xiang, W (2021). MicroRNAs secreted by human embryos could be potential biomarkers for clinical outcomes of assisted reproductive technology. Journal of Advanced Research 31, 25–34.
MicroRNAs secreted by human embryos could be potential biomarkers for clinical outcomes of assisted reproductive technology.Crossref | GoogleScholarGoogle Scholar | 34194830PubMed |

Feng, R, Sang, Q, Zhu, Y, Fu, W, Liu, M, Xu, Y, Shi, H, Xu, Y, Qu, R, Chai, R, Shao, R, Jin, L, He, L, Sun, X, and Wang, L (2015). MiRNA-320 in the human follicular fluid is associated with embryo quality in vivo and affects mouse embryonic development in vitro. Scientific Reports 5, 8689.
MiRNA-320 in the human follicular fluid is associated with embryo quality in vivo and affects mouse embryonic development in vitro.Crossref | GoogleScholarGoogle Scholar | 25732513PubMed |

Ferraretti, AP, Goossens, V, de Mouzon, J, Bhattacharya, S, Castilla, JA, Korsak, V, Kupka, M, Nygren, KG, and Nyboe Andersen, A Ferraretti, AP, Goossens, V, de Mouzon, J, Bhattacharya, S, Castilla, JA, Korsak, V, Kupka, M, Nygren, KG, and Nyboe Andersen, A Ferraretti, AP, Goossens, V, de Mouzon, J, Bhattacharya, S, Castilla, JA, Korsak, V, Kupka, M, Nygren, KG, and Nyboe Andersen, A (2012). Assisted reproductive technology in Europe, 2008: results generated from European registers by ESHRE. Human Reproduction 27, 2571–2584.
Assisted reproductive technology in Europe, 2008: results generated from European registers by ESHRE.Crossref | GoogleScholarGoogle Scholar | 22786779PubMed |

Galliano, D, and Pellicer, A (2014). MicroRNA and implantation. Fertility and Sterility 101, 1531–1544.
MicroRNA and implantation.Crossref | GoogleScholarGoogle Scholar | 24882617PubMed |

García-López, J, and del Mazo, J (2012). Expression dynamics of microRNA biogenesis during preimplantation mouse development. Biochimica et Biophysica Acta (BBA) – Gene Regulatory Mechanisms 1819, 847–854.
Expression dynamics of microRNA biogenesis during preimplantation mouse development.Crossref | GoogleScholarGoogle Scholar |

Giacomini, E, Vago, R, Sanchez, AM, Podini, P, Zarovni, N, Murdica, V, Rizzo, R, Bortolotti, D, Candiani, M, and Viganò, P (2017). Secretome of in vitro cultured human embryos contains extracellular vesicles that are uptaken by the maternal side. Scientific Reports 7, 5210.
Secretome of in vitro cultured human embryos contains extracellular vesicles that are uptaken by the maternal side.Crossref | GoogleScholarGoogle Scholar | 28701751PubMed |

Giraldez, AJ, Mishima, Y, Rihel, J, Grocock, RJ, Van Dongen, S, Inoue, K, Enright, AJ, and Schier, AF (2006). Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312, 75–79.
Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs.Crossref | GoogleScholarGoogle Scholar | 16484454PubMed |

Gross, N, Kropp, J, and Khatib, H (2017a). MicroRNA signaling in embryo development. Biology 6, 34.
MicroRNA signaling in embryo development.Crossref | GoogleScholarGoogle Scholar |

Gross, N, Kropp, J, and Khatib, H (2017b). Sexual dimorphism of miRNAs secreted by bovine in vitro-produced embryos. Frontiers in Genetics 8, 39.
Sexual dimorphism of miRNAs secreted by bovine in vitro-produced embryos.Crossref | GoogleScholarGoogle Scholar | 28421107PubMed |

Kim, K-H, Seo, Y-M, Kim, E-Y, Lee, S-Y, Kwon, J, Ko, J-J, and Lee, K-A (2016). The miR-125 family is an important regulator of the expression and maintenance of maternal effect genes during preimplantational embryo development. Open Biology 6, 160181.
The miR-125 family is an important regulator of the expression and maintenance of maternal effect genes during preimplantational embryo development.Crossref | GoogleScholarGoogle Scholar | 27906131PubMed |

Kirkegaard, K, Yan, Y, Sørensen, BS, Hardarson, T, Hanson, C, Ingerslev, HJ, Knudsen, UB, Kjems, J, Lundin, K, and Ahlström, A (2020). Comprehensive analysis of soluble RNAs in human embryo culture media and blastocoel fluid. Journal of Assisted Reproduction and Genetics 37, 2199–2209.
Comprehensive analysis of soluble RNAs in human embryo culture media and blastocoel fluid.Crossref | GoogleScholarGoogle Scholar | 32681282PubMed |

Kropp, J, and Khatib, H (2015). Characterization of microRNA in bovine in vitro culture media associated with embryo quality and development. Journal of Dairy Science 98, 6552–6563.
Characterization of microRNA in bovine in vitro culture media associated with embryo quality and development.Crossref | GoogleScholarGoogle Scholar | 26142856PubMed |

Kropp, J, Salih, SM, and Khatib, H (2014). Expression of microRNAs in bovine and human pre-implantation embryo culture media. Frontiers in Genetics 5, 91.
Expression of microRNAs in bovine and human pre-implantation embryo culture media.Crossref | GoogleScholarGoogle Scholar | 24795753PubMed |

Laurent, LC (2008). MicroRNAs in embryonic stem cells and early embryonic development. Journal of Cellular and Molecular Medicine 12, 2181–2188.
MicroRNAs in embryonic stem cells and early embryonic development.Crossref | GoogleScholarGoogle Scholar | 19120702PubMed |

Lee, MT, Bonneau, AR, and Giraldez, AJ (2014). Zygotic genome activation during the maternal-to-zygotic transition. Annual Review of Cell and Developmental Biology 30, 581–613.
Zygotic genome activation during the maternal-to-zygotic transition.Crossref | GoogleScholarGoogle Scholar | 25150012PubMed |

Liang, J, Wang, S, and Wang, Z (2017). Role of microRNAs in embryo implantation. Reproductive Biology and Endocrinology: RB&E 15, 90.
Role of microRNAs in embryo implantation.Crossref | GoogleScholarGoogle Scholar |

Lin, X, Beckers, E, Mc Cafferty, S, Gansemans, Y, Joanna Szymańska, K, Chaitanya Pavani, K, Catani, JP, Van Nieuwerburgh, F, Deforce, D, De Sutter, P, Van Soom, A, and Peelman, L (2019). Bovine embryo-secreted microRNA-30c is a potential non-invasive biomarker for hampered preimplantation developmental competence. Frontiers in Genetics 10, 315.
Bovine embryo-secreted microRNA-30c is a potential non-invasive biomarker for hampered preimplantation developmental competence.Crossref | GoogleScholarGoogle Scholar | 31024625PubMed |

Liu, W-M, Pang, RTK, Chiu, PCN, Wong, BPC, Lao, K, Lee, K-F, and Yeung, WSB (2012a). Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proceedings of the National Academy of Sciences of the United States of America 109, 490–494.
Sperm-borne microRNA-34c is required for the first cleavage division in mouse.Crossref | GoogleScholarGoogle Scholar | 22203953PubMed |

Liu, WM, Pang, RTK, Cheong, AWY, Ng, EHY, Lao, K, Lee, K-F, and Yeung, WSB (2012b). Involvement of microRNA lethal-7a in the regulation of embryo implantation in mice. PLoS ONE 7, e37039.
Involvement of microRNA lethal-7a in the regulation of embryo implantation in mice.Crossref | GoogleScholarGoogle Scholar | 22623977PubMed |

Liu, W, Niu, Z, Li, Q, Pang, RTK, Chiu, PCN, and Yeung, WS-B (2016). MicroRNA and embryo implantation. American Journal of Reproductive Immunology 75, 263–271.
MicroRNA and embryo implantation.Crossref | GoogleScholarGoogle Scholar | 26707514PubMed |

Machtinger, R, Rodosthenous, RS, Adir, M, Mansour, A, Racowsky, C, Baccarelli, AA, and Hauser, R (2017). Extracellular microRNAs in follicular fluid and their potential association with oocyte fertilization and embryo quality: an exploratory study. Journal of Assisted Reproduction and Genetics 34, 525–533.
Extracellular microRNAs in follicular fluid and their potential association with oocyte fertilization and embryo quality: an exploratory study.Crossref | GoogleScholarGoogle Scholar | 28188594PubMed |

Makri, D, Efstathiou, P, Michailidou, E, and Maalouf, WE (2020). Apoptosis triggers the release of microRNA miR-294 in spent culture media of blastocysts. Journal of Assisted Reproduction and Genetics 37, 1685–1694.
Apoptosis triggers the release of microRNA miR-294 in spent culture media of blastocysts.Crossref | GoogleScholarGoogle Scholar | 32440932PubMed |

Martinez, RM, Liang, L, Racowsky, C, Dioni, L, Mansur, A, Adir, M, Bollati, V, Baccarelli, AA, Hauser, R, and Machtinger, R (2018). Extracellular microRNAs profile in human follicular fluid and IVF outcomes. Scientific Reports 8, 17036.
Extracellular microRNAs profile in human follicular fluid and IVF outcomes.Crossref | GoogleScholarGoogle Scholar | 30451969PubMed |

Medeiros, LA, Dennis, LM, Gill, ME, Houbaviy, H, Markoulaki, S, Fu, D, White, AC, Kirak, O, Sharp, PA, Page, DC, and Jaenisch, R (2011). Mir-290-295 deficiency in mice results in partially penetrant embryonic lethality and germ cell defects. Proceedings of the National Academy of Sciences of the United States of America 108, 14163–14168.
Mir-290-295 deficiency in mice results in partially penetrant embryonic lethality and germ cell defects.Crossref | GoogleScholarGoogle Scholar | 21844366PubMed |

Melo-Baez, B, Wong, YS, Aguilera, CJ, Cabezas, J, Mançanares, ACF, Riadi, G, Castro, FO, and Rodriguez-Alvarez, L (2020). MicroRNAs from extracellular vesicles secreted by bovine embryos as early biomarkers of developmental competence. International Journal of Molecular Sciences 21, 8888.
MicroRNAs from extracellular vesicles secreted by bovine embryos as early biomarkers of developmental competence.Crossref | GoogleScholarGoogle Scholar |

Palini, S, Galluzzi, L, De Stefani, S, Bianchi, M, Wells, D, Magnani, M, and Bulletti, C (2013). Genomic DNA in human blastocoele fluid. Reproductive BioMedicine Online 26, 603–610.
Genomic DNA in human blastocoele fluid.Crossref | GoogleScholarGoogle Scholar | 23557766PubMed |

Parchem, RJ, Moore, N, Fish, JL, Parchem, JG, Braga, TT, Shenoy, A, Oldham, MC, Rubenstein, JL, Schneider, RA, and Blelloch, R (2015). miR-302 is required for timing of neural differentiation, neural tube closure, and embryonic viability. Cell Reports 12, 760–773.
miR-302 is required for timing of neural differentiation, neural tube closure, and embryonic viability.Crossref | GoogleScholarGoogle Scholar | 26212322PubMed |

Rio, PD, and Madan, P (2021). Does miRNA expression in the spent media change during early embryo development? Frontiers in Veterinary Science 8, 319.
Does miRNA expression in the spent media change during early embryo development?Crossref | GoogleScholarGoogle Scholar |

Rødgaard, T, Heegaard, PMH, and Callesen, H (2015). Non-invasive assessment of in-vitro embryo quality to improve transfer success. Reproductive BioMedicine Online 31, 585–592.
Non-invasive assessment of in-vitro embryo quality to improve transfer success.Crossref | GoogleScholarGoogle Scholar | 26380864PubMed |

Rosenbluth, EM, Shelton, DN, Sparks, AET, Devor, E, Christenson, L, and Van Voorhis, BJ (2013). MicroRNA expression in the human blastocyst. Fertility and Sterility 99, 855–861.e3.
MicroRNA expression in the human blastocyst.Crossref | GoogleScholarGoogle Scholar | 23211712PubMed |

Rosenbluth, EM, Shelton, DN, Wells, LM, Sparks, AET, and Van Voorhis, BJ (2014). Human embryos secrete microRNAs into culture media – a potential biomarker for implantation. Fertility and Sterility 101, 1493–1500.
Human embryos secrete microRNAs into culture media – a potential biomarker for implantation.Crossref | GoogleScholarGoogle Scholar | 24786747PubMed |

Salilew-Wondim, D, Gebremedhn, S, Hoelker, M, Tholen, E, Hailay, T, and Tesfaye, D (2020). The role of microRNAs in mammalian fertility: from gametogenesis to embryo implantation. International Journal of Molecular Sciences 21, 585.
The role of microRNAs in mammalian fertility: from gametogenesis to embryo implantation.Crossref | GoogleScholarGoogle Scholar |

Simon, A, and Laufer, N (2012). Assessment and treatment of repeated implantation failure (RIF). Journal of Assisted Reproduction and Genetics 29, 1227–1239.
Assessment and treatment of repeated implantation failure (RIF).Crossref | GoogleScholarGoogle Scholar | 22976427PubMed |

Sinha, PB, Tesfaye, D, Rings, F, Hossien, M, Hoelker, M, Held, E, Neuhoff, C, Tholen, E, Schellander, K, and Salilew-Wondim, D (2017). MicroRNA-130b is involved in bovine granulosa and cumulus cells function, oocyte maturation and blastocyst formation. Journal of Ovarian Research 10, 37.
MicroRNA-130b is involved in bovine granulosa and cumulus cells function, oocyte maturation and blastocyst formation.Crossref | GoogleScholarGoogle Scholar | 28629378PubMed |

Sinkkonen, L, Hugenschmidt, T, Berninger, P, Gaidatzis, D, Mohn, F, Artus-Revel, CG, Zavolan, M, Svoboda, P, and Filipowicz, W (2008). MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nature Structural & Molecular Biology 15, 259–267.
MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar |

Subramanyam, D, Lamouille, S, Judson, RL, Liu, JY, Bucay, N, Derynck, R, and Blelloch, R (2011). Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nature Biotechnology 29, 443–448.
Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 21490602PubMed |

Svoboda, P, and Flemr, M (2010). The role of miRNAs and endogenous siRNAs in maternal-to-zygotic reprogramming and the establishment of pluripotency. EMBO Reports 11, 590–597.
The role of miRNAs and endogenous siRNAs in maternal-to-zygotic reprogramming and the establishment of pluripotency.Crossref | GoogleScholarGoogle Scholar | 20651740PubMed |

Tan, K, Wang, X, Zhang, Z, Miao, K, Yu, Y, An, L, and Tian, J (2016). Downregulation of miR-199a-5p disrupts the developmental potential of in vitro-fertilized mouse blastocysts. Biology of Reproduction 95, 54.
Downregulation of miR-199a-5p disrupts the developmental potential of in vitro-fertilized mouse blastocysts.Crossref | GoogleScholarGoogle Scholar | 27488027PubMed |

Tang, F, Kaneda, M, O’Carroll, D, Hajkova, P, Barton, SC, Sun, YA, Lee, C, Tarakhovsky, A, Lao, K, and Surani, MA (2007). Maternal microRNAs are essential for mouse zygotic development. Genes & Development 21, 644–648.
Maternal microRNAs are essential for mouse zygotic development.Crossref | GoogleScholarGoogle Scholar |

Tesfaye, D, Worku, D, Rings, F, Phatsara, C, Tholen, E, Schellander, K, and Hoelker, M (2009). Identification and expression profiling of microRNAs during bovine oocyte maturation using heterologous approach. Molecular Reproduction and Development 76, 665–677.
Identification and expression profiling of microRNAs during bovine oocyte maturation using heterologous approach.Crossref | GoogleScholarGoogle Scholar | 19170227PubMed |

Tscherner, A, Gilchrist, G, Smith, N, Blondin, P, Gillis, D, and LaMarre, J (2014). MicroRNA-34 family expression in bovine gametes and preimplantation embryos. Reproductive Biology and Endocrinology 12, 85.
MicroRNA-34 family expression in bovine gametes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 25179211PubMed |

Wang, M, Gao, Y, Qu, P, Qing, S, Qiao, F, Zhang, Y, Mager, J, and Wang, Y (2017). Sperm-borne miR-449b influences cleavage, epigenetic reprogramming and apoptosis of SCNT embryos in bovine. Scientific Reports 7, 13403.
Sperm-borne miR-449b influences cleavage, epigenetic reprogramming and apoptosis of SCNT embryos in bovine.Crossref | GoogleScholarGoogle Scholar | 29042680PubMed |

Wang, J-L, Zhang, C, Liu, B, Huang, X-M, Dai, J-G, Tian, J-H, and Gao, J-M (2019). Function of berberine on porcine in vitro fertilization embryo development and differential expression analysis of microRNAs. Reproduction in Domestic Animals 54, 520–530.
Function of berberine on porcine in vitro fertilization embryo development and differential expression analysis of microRNAs.Crossref | GoogleScholarGoogle Scholar | 30578596PubMed |

Wang, M, Du, Y, Gao, S, Wang, Z, Qu, P, Gao, Y, Wang, J, Liu, Z, Zhang, J, Zhang, Y, Qing, S, and Wang, Y (2021). Sperm-borne miR-202 targets SEPT7 and regulates first cleavage of bovine embryos via cytoskeletal remodeling. Development 148, dev.189670.
Sperm-borne miR-202 targets SEPT7 and regulates first cleavage of bovine embryos via cytoskeletal remodeling.Crossref | GoogleScholarGoogle Scholar |

Xu, H, Wang, X, Wang, Z, Li, J, Xu, Z, Miao, M, Chen, G, Lei, X, Wu, J, Shi, H, Wang, K, Zhang, T, and Sun, X (2020). MicroRNA expression profile analysis in sperm reveals hsa-mir-191 as an auspicious omen of in vitro fertilization. BMC Genomics 21, 165.
MicroRNA expression profile analysis in sperm reveals hsa-mir-191 as an auspicious omen of in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 32066367PubMed |

Yang, Y, Bai, W, Zhang, L, Yin, G, Wang, X, Wang, J, Zhao, H, Han, Y, and Yao, Y-Q (2008). Determination of microRNAs in mouse preimplantation embryos by microarray. Developmental Dynamics 237, 2315–2327.
Determination of microRNAs in mouse preimplantation embryos by microarray.Crossref | GoogleScholarGoogle Scholar | 18729214PubMed |

Yuan, S, Schuster, A, Tang, C, Yu, T, Ortogero, N, Bao, J, Zheng, H, and Yan, W (2016). Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development. Development 143, 635–647.
Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development.Crossref | GoogleScholarGoogle Scholar | 26718009PubMed |

Zamora, S, Clavero, A, Gonzalvo, MC, de Dios Luna Del Castillo, J, Roldán-Nofuentes, JA, Mozas, J, and Castilla, JA (2011). PGS-FISH in reproductive medicine and perspective directions for improvement: a systematic review. Journal of Assisted Reproduction and Genetics 28, 747–757.
PGS-FISH in reproductive medicine and perspective directions for improvement: a systematic review.Crossref | GoogleScholarGoogle Scholar | 21713549PubMed |

Zhang, C, Shi, Y-R, Liu, X-R, Cao, Y-C, Tian, J-L, Jia, Z-Y, Zhen, D, Liu, F-H, and Gao, J-M (2014). The regulatory role of icariin on apoptosis in mouse preimplantation embryos with reduced microRNA-21. Theriogenology 82, 461–468.
The regulatory role of icariin on apoptosis in mouse preimplantation embryos with reduced microRNA-21.Crossref | GoogleScholarGoogle Scholar | 24948525PubMed |

Zhou, W, and Dimitriadis, E (2020). Secreted microRNA to predict embryo implantation outcome: from research to clinical diagnostic application. Frontiers in Cell and Developmental Biology 8, 939.
Secreted microRNA to predict embryo implantation outcome: from research to clinical diagnostic application.Crossref | GoogleScholarGoogle Scholar |