Identification of differentially expressed microRNAs in outgrowth embryos compared with blastocysts and non-outgrowth embryos in mice
Jihyun Kim A B C * , Jaewang Lee B * and Jin Hyun Jun
B C D E
+ Author Affiliations
- Author Affiliations
A Clinical Medicine Division, Korea Institute of Oriental Medicine, 1672 Yuseong-daero, Yuseong-gu, Daejeon, 34054, Republic of Korea.
B Department of Biomedical Laboratory Science, Eulji University, 553 Sanseong-daero, Sujeong-gu, Seongnam-si, Gyeonggi-do 13135, Republic of Korea.
C Department of Senior Healthcare BK21 plus program, Graduate School of Eulji University, 553 Sanseong-daero, Sujeong-gu, Seongnam-si, Gyeonggi-do 13135, Republic of Korea.
D Eulji Medi-Bio Research Institute (EMBRI), Eulji University, 77 Gyeryong-ro 771Beon-gil, Jung-gu Daejeon, 34824, Republic of Korea.
E Corresponding author. Email: junjh55@hanmail.net
Reproduction, Fertility and Development 31(4) 645-657 https://doi.org/10.1071/RD18161
Submitted: 1 May 2018 Accepted: 6 October 2018 Published: 15 November 2018
Abstract
Recurrent implantation failure (RIF) is one of the main causes for the repeated failure of IVF, and the major reason for RIF is thought to be a miscommunication between the embryo and uterus. However, the exact mechanism underlying embryo–uterus cross-talk is not fully understood. The aim of the present study was to identify differentially expressed microRNAs (miRNAs) among blastocysts, non-outgrowth and outgrowth embryos in mice using microarray analysis. A bioinformatics analysis was performed to predict the potential mechanisms of implantation. The miRNA expression profiles differed significantly between non-outgrowth and outgrowth embryos. In all, 3163 miRNAs were detected in blastocysts and outgrowth embryos. Of these, 10 miRNA candidates (let-7b, miR-23a, miR-27a, miR-92a, miR-183, miR-200c, miR-291a, miR-425, miR-429 and miR-652) were identified as significant differentially expressed miRNAs of outgrowth embryos by in silico analysis. The expression of the miRNA candidates was markedly changed during preimplantation embryo development. In particular, let-7b-5p, miR-200c-3p and miR-23a-3p were significantly upregulated in outgrowth embryos compared with non-outgrowth blastocysts. Overall, differentially expressed miRNAs in outgrowth embryos compared with blastocysts and non-outgrowth embryos could be involved in embryo attachment, and interaction between the embryo proper and maternal endometrium during the implantation process.
Additional keywords: bioinformatics analysis, embryo implantation, microarray, miRNA profile.
References
Abu-Halima, M., Hausler, S., Backes, C., Fehlmann, T., Staib, C., Nestel, S., Nazarenko, I., Meese, E., and Keller, A. (2017). Micro-ribonucleic acids and extracellular vesicles repertoire in the spent culture media is altered in women undergoing in vitro fertilization. Sci. Rep. 7, 13525.| Micro-ribonucleic acids and extracellular vesicles repertoire in the spent culture media is altered in women undergoing in vitro fertilization.Crossref | GoogleScholarGoogle Scholar |
Al-Turki, H. A. (2018). Hysteroscopy as an investigation tool in recurrent implantation failure in vitro fertilization. Saudi Med. J. 39, 243–246.
| Hysteroscopy as an investigation tool in recurrent implantation failure in vitro fertilization.Crossref | GoogleScholarGoogle Scholar |
Bland, C. L., Byrne-Hoffman, C. N., Fernandez, A., Rellick, S. L., Deng, W., and Klinke, D. J. (2018). Exosomes derived from B16F0 melanoma cells alter the transcriptome of cytotoxic T cells that impacts mitochondrial respiration. FEBS J. 285, 1033–1050.
| Exosomes derived from B16F0 melanoma cells alter the transcriptome of cytotoxic T cells that impacts mitochondrial respiration.Crossref | GoogleScholarGoogle Scholar |
Bruzzone, R., White, T. W., and Paul, D. L. (1996). Connections with connexins: the molecular basis of direct intercellular signaling. Eur. J. Biochem. 238, 1–27.
| Connections with connexins: the molecular basis of direct intercellular signaling.Crossref | GoogleScholarGoogle Scholar |
Cai, L. Q., Cao, Y. J., and Duan, E. K. (2000). Effects of leukaemia inhibitory factor on embryo implantation in the mouse. Cytokine 12, 1676–1682.
| Effects of leukaemia inhibitory factor on embryo implantation in the mouse.Crossref | GoogleScholarGoogle Scholar |
Camussi, G., Deregibus, M. C., Bruno, S., Grange, C., Fonsato, V., and Tetta, C. (2011). Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am. J. Cancer Res. 1, 98–110.
Chen, Y., Liersch, R., and Detmar, M. (2012). The miR-290–295 cluster suppresses autophagic cell death of melanoma cells. Sci. Rep. 2, 808.
| The miR-290–295 cluster suppresses autophagic cell death of melanoma cells.Crossref | GoogleScholarGoogle Scholar |
Cheong, A. W., Pang, R. T., Liu, W. M., Kottawatta, K. S., Lee, K. F., and Yeung, W. S. (2014). MicroRNA Let-7a and dicer are important in the activation and implantation of delayed implanting mouse embryos. Hum. Reprod. 29, 750–762.
| MicroRNA Let-7a and dicer are important in the activation and implantation of delayed implanting mouse embryos.Crossref | GoogleScholarGoogle Scholar |
Choteau, S. A., Cuesta Torres, L. F., Barraclough, J. Y., Elder, A. M. M., Martinez, G. J., Chen Fan, W. Y., Shrestha, S., Ong, K. L., Barter, P. J., Celermajer, D. S., Rye, K. A., Patel, S., and Tabet, F. (2018). Transcoronary gradients of HDL-associated microRNAs in unstable coronary artery disease. Int. J. Cardiol. 253, 138–144.
| Transcoronary gradients of HDL-associated microRNAs in unstable coronary artery disease.Crossref | GoogleScholarGoogle Scholar |
Chu, B., Zhong, L., Dou, S., Wang, J., Li, J., Wang, M., Shi, Q., Mei, Y., and Wu, M. (2015). miRNA-181 regulates embryo implantation in mice through targeting leukemia inhibitory factor. J. Mol. Cell Biol. 7, 12–22.
| miRNA-181 regulates embryo implantation in mice through targeting leukemia inhibitory factor.Crossref | GoogleScholarGoogle Scholar |
Chung, T. W., Park, M. J., Kim, H. S., Choi, H. J., and Ha, K. T. (2016). Integrin alphaVbeta3 and alphaVbeta5 are required for leukemia inhibitory factor-mediated the adhesion of trophoblast cells to the endometrial cells. Biochem. Biophys. Res. Commun. 469, 936–940.
| Integrin alphaVbeta3 and alphaVbeta5 are required for leukemia inhibitory factor-mediated the adhesion of trophoblast cells to the endometrial cells.Crossref | GoogleScholarGoogle Scholar |
Coughlan, C., Ledger, W., Wang, Q., Liu, F., Demirol, A., Gurgan, T., Cutting, R., Ong, K., Sallam, H., and Li, T. C. (2014). Recurrent implantation failure: definition and management. Reprod. Biomed. Online 28, 14–38.
| Recurrent implantation failure: definition and management.Crossref | GoogleScholarGoogle Scholar |
Da Silveira, J., Andrade, G. M., Perecin, F., Meireles, F. V., Winger, Q. A., and Bouma, G. J. (2018). Isolation and analysis of exosomal microRNAs from ovarian follicular fluid. Methods Mol. Biol. 1733, 53–63.
| Isolation and analysis of exosomal microRNAs from ovarian follicular fluid.Crossref | GoogleScholarGoogle Scholar |
DaSilva-Arnold, S. C., Zamudio, S., Al-Khan, A., Alvarez-Perez, J., Mannion, C., Koenig, C., Luke, D., Perez, A. M., Petroff, M., Alvarez, M., and Illsley, N. P. (2018). Human trophoblast epithelial–mesenchymal transition in abnormally invasive placenta. Biol. Reprod. 99, 409–421.
| Human trophoblast epithelial–mesenchymal transition in abnormally invasive placenta.Crossref | GoogleScholarGoogle Scholar |
de Jong, O. G., Verhaar, M. C., Chen, Y., Vader, P., Gremmels, H., Posthuma, G., Schiffelers, R. M., Gucek, M., and van Balkom, B. W. (2012). Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J. Extracell. Vesicles 1, 1.
| Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes.Crossref | GoogleScholarGoogle Scholar |
Fang, T., Lv, H., Lv, G., Li, T., Wang, C., Han, Q., Yu, L., Su, B., Guo, L., Huang, S., Cao, D., Tang, L., Tang, S., Wu, M., Yang, W., and Wang, H. (2018). Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat. Commun. 9, 191.
| Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer.Crossref | GoogleScholarGoogle Scholar |
Farimani, M., Poorolajal, J., Rabiee, S., and Bahmanzadeh, M. (2017). Successful pregnancy and live birth after intrauterine administration of autologous platelet-rich plasma in a woman with recurrent implantation failure: a case report. Int. J. Reprod. Biomed. (Yazd) 15, 803–806.
| Successful pregnancy and live birth after intrauterine administration of autologous platelet-rich plasma in a woman with recurrent implantation failure: a case report.Crossref | GoogleScholarGoogle Scholar |
Galliano, D., and Pellicer, A. (2014). MicroRNA and implantation. Fertil. Steril. 101, 1531–1544.
| MicroRNA and implantation.Crossref | GoogleScholarGoogle Scholar |
Gomes, A. Q., Nolasco, S., and Soares, H. (2013). Non-coding RNAs: multi-tasking molecules in the cell. Int. J. Mol. Sci. 14, 16010–16039.
| Non-coding RNAs: multi-tasking molecules in the cell.Crossref | GoogleScholarGoogle Scholar |
Gross, N., Kropp, J., and Khatib, H. (2017). MicroRNA signaling in embryo development. Biology (Basel) 6, .
Guo, L., and Lu, Z. (2010). Global expression analysis of miRNA gene cluster and family based on isomiRs from deep sequencing data. Comput. Biol. Chem. 34, 165–171.
| Global expression analysis of miRNA gene cluster and family based on isomiRs from deep sequencing data.Crossref | GoogleScholarGoogle Scholar |
Guo, C., Zhao, D., Zhang, Q., Liu, S., and Sun, M.-Z. (2018). miR-429 suppresses tumor migration and invasion by targeting CRKL in hepatocellular carcinoma via inhibiting Raf/MEK/ERK pathway and epithelial-mesenchymal transition. Sci. Rep. 8, 2375.
| miR-429 suppresses tumor migration and invasion by targeting CRKL in hepatocellular carcinoma via inhibiting Raf/MEK/ERK pathway and epithelial-mesenchymal transition.Crossref | GoogleScholarGoogle Scholar |
Ham, O., Lee, S. Y., Lee, C. Y., Park, J. H., Lee, J., Seo, H. H., Cha, M. J., Choi, E., Kim, S., and Hwang, K. C. (2015). let-7b suppresses apoptosis and autophagy of human mesenchymal stem cells transplanted into ischemia/reperfusion injured heart 7by targeting caspase-3. Stem Cell Res. Ther. 6, 147.
| let-7b suppresses apoptosis and autophagy of human mesenchymal stem cells transplanted into ischemia/reperfusion injured heart 7by targeting caspase-3.Crossref | GoogleScholarGoogle Scholar |
Hosseini, M. K., Gunel, T., Gumusoglu, E., Benian, A., and Aydinli, K. (2018). MicroRNA expression profiling in placenta and maternal plasma in early pregnancy loss. Mol. Med. Rep. 17, 4941–4952.
Houbaviy, H. B., Murray, M. F., and Sharp, P. A. (2003). Embryonic stem cell-specific microRNAs. Dev. Cell 5, 351–358.
| Embryonic stem cell-specific microRNAs.Crossref | GoogleScholarGoogle Scholar |
Inyawilert, W., Fu, T. Y., Lin, C. T., and Tang, P. C. (2015). Let-7-mediated suppression of mucin 1 expression in the mouse uterus during embryo implantation. J. Reprod. Dev. 61, 138–144.
| Let-7-mediated suppression of mucin 1 expression in the mouse uterus during embryo implantation.Crossref | GoogleScholarGoogle Scholar |
Kojima, T., Murata, M., Go, M., Spray, D. C., and Sawada, N. (2007). Connexins induce and maintain tight junctions in epithelial cells. J. Membr. Biol. 217, 13–19.
| Connexins induce and maintain tight junctions in epithelial cells.Crossref | GoogleScholarGoogle Scholar |
Kovacs, P. (2014). Embryo selection: the role of time-lapse monitoring. Reprod. Biol. Endocrinol. 12, 124.
| Embryo selection: the role of time-lapse monitoring.Crossref | GoogleScholarGoogle Scholar |
Kumar, P., Luo, Y., Tudela, C., Alexander, J. M., and Mendelson, C. R. (2013). The c-Myc-regulated microRNA-17~92 (miR-17~92) and miR-106a~363 clusters target hCYP19A1 and hGCM1 to inhibit human trophoblast differentiation. Mol. Cell. Biol. 33, 1782–1796.
| The c-Myc-regulated microRNA-17~92 (miR-17~92) and miR-106a~363 clusters target hCYP19A1 and hGCM1 to inhibit human trophoblast differentiation.Crossref | GoogleScholarGoogle Scholar |
Li, Z., Gou, J., Jia, J., and Zhao, X. (2015). MicroRNA-429 functions as a regulator of epithelial–mesenchymal transition by targeting Pcdh8 during murine embryo implantation. Hum. Reprod. 30, 507–518.
| MicroRNA-429 functions as a regulator of epithelial–mesenchymal transition by targeting Pcdh8 during murine embryo implantation.Crossref | GoogleScholarGoogle Scholar |
Liang, J., Wang, S., and Wang, Z. (2017). Role of microRNAs in embryo implantation. Reprod. Biol. Endocrinol. 15, 90.
| Role of microRNAs in embryo implantation.Crossref | GoogleScholarGoogle Scholar |
Lichner, Z., Pall, E., Kerekes, A., Pallinger, E., Maraghechi, P., Bosze, Z., and Gocza, E. (2011). The miR-290–295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells. Differentiation 81, 11–24.
| The miR-290–295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar |
Liu, W. M., Pang, R. T., Cheong, A. W., Ng, E. H., Lao, K., Lee, K. F., and Yeung, W. S. (2012a). 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 |
Liu, W. M., Zhang, F., Moshiach, S., Zhou, B., Huang, C., Srinivasan, K., Khurana, S., Zheng, Y., Lahti, J. M., and Zhang, X. A. (2012b). Tetraspanin CD82 inhibits protrusion and retraction in cell movement by attenuating the plasma membrane-dependent actin organization. PLoS One 7, e51797.
| Tetraspanin CD82 inhibits protrusion and retraction in cell movement by attenuating the plasma membrane-dependent actin organization.Crossref | GoogleScholarGoogle Scholar |
Liu, Y., Liu, Q., Jia, W., Chen, J., Wang, J., Ye, D., Guo, X., Chen, W., Li, G., Wang, G., Deng, A., and Kang, J. (2013). MicroRNA-200a regulates Grb2 and suppresses differentiation of mouse embryonic stem cells into endoderm and mesoderm. PLoS One 8, e68990.
| MicroRNA-200a regulates Grb2 and suppresses differentiation of mouse embryonic stem cells into endoderm and mesoderm.Crossref | GoogleScholarGoogle Scholar |
Ma, J., Liu, J., Wang, Z., Gu, X., Fan, Y., Zhang, W., Xu, L., Zhang, J., and Cai, D. (2014). NF-kappaB-dependent microRNA-425 upregulation promotes gastric cancer cell growth by targeting PTEN upon IL-1beta induction. Mol. Cancer 13, 40.
| NF-kappaB-dependent microRNA-425 upregulation promotes gastric cancer cell growth by targeting PTEN upon IL-1beta induction.Crossref | GoogleScholarGoogle Scholar |
Machtinger, R., Laurent, L. C., and Baccarelli, A. A. (2016). Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Hum. Reprod. Update 22, 182–193.
Magenta, A., Cencioni, C., Fasanaro, P., Zaccagnini, G., Greco, S., Sarra-Ferraris, G., Antonini, A., Martelli, F., and Capogrossi, M. C. (2011). miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ. 18, 1628–1639.
| miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition.Crossref | GoogleScholarGoogle Scholar |
Mathieu, J., and Ruohola-Baker, H. (2013). Regulation of stem cell populations by microRNAs. Adv. Exp. Med. Biol. 786, 329–351.
| Regulation of stem cell populations by microRNAs.Crossref | GoogleScholarGoogle Scholar |
Mathivanan, S., and Simpson, R. J. (2009). ExoCarta: a compendium of exosomal proteins and RNA. Proteomics 9, 4997–5000.
| ExoCarta: a compendium of exosomal proteins and RNA.Crossref | GoogleScholarGoogle Scholar |
Mathivanan, S., Ji, H., and Simpson, R. J. (2010). Exosomes: extracellular organelles important in intercellular communication. J. Proteomics 73, 1907–1920.
| Exosomes: extracellular organelles important in intercellular communication.Crossref | GoogleScholarGoogle Scholar |
Mercer, T. R., and Mattick, J. S. (2013). Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 20, 300–307.
| Structure and function of long noncoding RNAs in epigenetic regulation.Crossref | GoogleScholarGoogle Scholar |
Paria, B. C., Song, H., and Dey, S. K. (2001). Implantation: molecular basis of embryo-uterine dialogue. Int. J. Dev. Biol. 45, 597–605.
Peng, F., Zhang, Y., Wang, R., Zhou, W., Zhao, Z., Liang, H., Qi, L., Zhao, W., Wang, H., Wang, C., Guo, Z., and Gu, Y. (2016). Identification of differentially expressed miRNAs in individual breast cancer patient and application in personalized medicine. Oncogenesis 5, e194.
| Identification of differentially expressed miRNAs in individual breast cancer patient and application in personalized medicine.Crossref | GoogleScholarGoogle Scholar |
Perkel, J. M. (2013). Assume nothing: the tale of circular RNA. Biotechniques 55, 55–57.
| Assume nothing: the tale of circular RNA.Crossref | GoogleScholarGoogle Scholar |
Pillai, R. S., Bhattacharyya, S. N., and Filipowicz, W. (2007). Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol. 17, 118–126.
| Repression of protein synthesis by miRNAs: how many mechanisms?Crossref | GoogleScholarGoogle Scholar |
Rosenbluth, E. M., Shelton, D. N., Wells, L. M., Sparks, A. E., and Van Voorhis, B. J. (2014). Human embryos secrete microRNAs into culture media – a potential biomarker for implantation. Fertil. Steril. 101, 1493–1500.
| Human embryos secrete microRNAs into culture media – a potential biomarker for implantation.Crossref | GoogleScholarGoogle Scholar |
Sebastian-Leon, P., Garrido, N., Remohi, J., Pellicer, A., and Diaz-Gimeno, P. (2018). Asynchronous and pathological windows of implantation: two causes of recurrent implantation failure. Hum. Reprod. 33, 626–635.
| Asynchronous and pathological windows of implantation: two causes of recurrent implantation failure.Crossref | GoogleScholarGoogle Scholar |
Steptoe, P. C., and Edwards, R. G. (1978). Birth after the reimplantation of a human embryo. Lancet 312, 366.
| Birth after the reimplantation of a human embryo.Crossref | GoogleScholarGoogle Scholar |
Tesfaye, D., Gebremedhn, S., Salilew-Wondim, D., Hailay, T., Hoelker, M., Grosse-Brinkhaus, C., and Schellander, K. (2018). MicroRNAs: tiny molecules with a significant role in mammalian follicular and oocyte development. Reproduction 155, R121–R135.
| MicroRNAs: tiny molecules with a significant role in mammalian follicular and oocyte development.Crossref | GoogleScholarGoogle Scholar |
Turchinovich, A., Weiz, L., and Burwinkel, B. (2012). Extracellular miRNAs: the mystery of their origin and function. Trends Biochem. Sci. 37, 460–465.
| Extracellular miRNAs: the mystery of their origin and function.Crossref | GoogleScholarGoogle Scholar |
Vidigal, J. A., and Ventura, A. (2012). Embryonic stem cell miRNAs and their roles in development and disease. Semin. Cancer Biol. 22, 428–436.
| Embryonic stem cell miRNAs and their roles in development and disease.Crossref | GoogleScholarGoogle Scholar |
Virant-Klun, I., Bui, H. T., and Ratajczak, M. Z. (2016a). Challenges in translating germinal stem cell research and therapy. Stem Cells Int. 2016, 4687378.
| Challenges in translating germinal stem cell research and therapy.Crossref | GoogleScholarGoogle Scholar |
Virant-Klun, I., Stahlberg, A., Kubista, M., and Skutella, T. (2016b). MicroRNAs: from female fertility, germ cells, and stem cells to cancer in humans. Stem Cells Int. 2016, 3984937.
| MicroRNAs: from female fertility, germ cells, and stem cells to cancer in humans.Crossref | GoogleScholarGoogle Scholar |
Viswanathan, S. R., Daley, G. Q., and Gregory, R. I. (2008). Selective blockade of microRNA processing by Lin28. Science 320, 97–100.
| Selective blockade of microRNA processing by Lin28.Crossref | GoogleScholarGoogle Scholar |
Xie, H., Tranguch, S., Jia, X., Zhang, H., Das, S. K., Dey, S. K., Kuo, C. J., and Wang, H. (2008). Inactivation of nuclear Wnt–beta-catenin signaling limits blastocyst competency for implantation. Development 135, 717–727.
| Inactivation of nuclear Wnt–beta-catenin signaling limits blastocyst competency for implantation.Crossref | GoogleScholarGoogle Scholar |
Yu, Z., Jian, Z., Shen, S. H., Purisima, E., and Wang, E. (2007). Global analysis of microRNA target gene expression reveals that miRNA targets are lower expressed in mature mouse and Drosophila tissues than in the embryos. Nucleic Acids Res. 35, 152–164.
| Global analysis of microRNA target gene expression reveals that miRNA targets are lower expressed in mature mouse and Drosophila tissues than in the embryos.Crossref | GoogleScholarGoogle Scholar |
Zheng, Q., Zhang, D., Yang, Y. U., Cui, X., Sun, J., Liang, C., Qin, H., Yang, X., Liu, S., and Yan, Q. (2017). MicroRNA-200c impairs uterine receptivity formation by targeting FUT4 and alpha1,3-fucosylation. Cell Death Differ. 24, 2161–2172.
| MicroRNA-200c impairs uterine receptivity formation by targeting FUT4 and alpha1,3-fucosylation.Crossref | GoogleScholarGoogle Scholar |
