Profiling bovine blastocyst microRNAs using deep sequencing
R. Pasquariello A G , B. Fernandez-Fuertes B , F. Strozzi C , F. Pizzi D , R. Mazza E , P. Lonergan B , F. Gandolfi A and J. L. Williams F
+ Author Affiliations
- Author Affiliations
A Dipartimento di Scienze Agrarie e Ambientali – Produzione, Territori, Università degli Studi di Milano, Via Celoria 2, 20133, Milan, Italy.
B School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Dublin, Ireland.
C Parco Tecnologico Padano, Via Einstein Albert, 26900, Lodi, Italy.
D Istituto di Biologia e Biotecnologia Agraria – Consiglio Nazionale delle Ricerche, Via Einstein Albert, 26900, Lodi, Italy.
E Associazione Italiana Allevatori, Via Bergamo 292, 26100, Cremona, Italy.
F School of Animal and Veterinary Sciences, Faculty of Science, University of Adelaide, Roseworthy, SA 5371, Australia.
G Corresponding author. Email: rolando.pasquariello@libero.it
Reproduction, Fertility and Development 29(8) 1545-1555 https://doi.org/10.1071/RD16110
Submitted: 8 March 2016 Accepted: 24 June 2016 Published: 13 September 2016
Abstract
MicroRNAs (miRNAs) are known to control several reproductive functions, including oocyte maturation, implantation and early embryonic development. Recent advances in deep sequencing have allowed the analysis of all miRNAs of a sample. However, when working with embryos, due to the low RNA content, miRNA profiling is challenging because of the relatively large amount of total RNA required for library preparation protocols. In the present study we compared three different procedures for RNA extraction and prepared libraries using pools of 30 bovine blastocysts. In total, 14 of the 15 most abundantly expressed miRNAs were common to all three procedures. Furthermore, using miRDeep discovery and annotation software (Max Delbrück Center), we identified 1363 miRNA sequences, of which bta-miR-10b and bta-miR-378 were the most abundant. Most of the 179 genes identified as experimentally validated (86.6%) or predicted targets (13.4%) were associated with cancer canonical pathways. We conclude that reliable analysis of bovine blastocyst miRNAs can be achieved using the procedures described herein. The repeatability of the results across different procedures and independent replicates, as well as their consistency with results obtained in other species, support the biological relevance of these miRNAs and of the gene pathways they modulate in early embryogenesis.
Additional keywords: epigenetics, gene regulation, RNA.
References
Abd El Naby, W. S., Hagos, T. H., Hossain, M. M., Salilew-Wondim, D., Gad, A. Y., Rings, F., Cinar, M. U., Tholen, E., Looft, C., Schellander, K., Hoelker, M., and Tesfaye, D. (2013). Expression analysis of regulatory microRNAs in bovine cumulus oocyte complex and preimplantation embryos. Zygote 21, 31–51.| Expression analysis of regulatory microRNAs in bovine cumulus oocyte complex and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVamtb4%3D&md5=e650ad0da628743113b224f9cab99c3cCAS | 22008281PubMed |
Bar, M., Wyman, S. K., Fritz, B. R., Qi, J., Garg, K. S., Parkin, R. K., Kroh, E. M., Bendoraite, A., Mitchell, P. S., Nelson, A. M., Ruzzo, W. L., Ware, C., Radich, J. P., Gentleman, R., Ruohola-Baker, H., and Tewari, M. (2008). MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries. Stem Cells 26, 2496–2505.
| MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlyku7rP&md5=ce592ba36cd35966693b2539543ed2c8CAS | 18583537PubMed |
Betoni, J. S., Derr, K., Pahl, M. C., Rogers, L., Muller, C. L., Packard, R. E., Carey, D. J., Kuivaniemi, H., and Tromp, G. (2013). MicroRNA analysis in placentas from patients with preeclampsia: comparison of new and published results. Hypertens. Pregnancy 32, 321–339.
| MicroRNA analysis in placentas from patients with preeclampsia: comparison of new and published results.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFerurrE&md5=b8bb860caf860dfee439d82e9b1c4314CAS | 23844600PubMed |
Braga, D. P., Setti, A. S., Figueira, R. C., Iaconelli, A., and Borges, E. (2014). The importance of the cleavage stage morphology evaluation for blastocyst transfer in patients with good prognosis. J. Assist. Reprod. Genet. 31, 1105–1110.
| The importance of the cleavage stage morphology evaluation for blastocyst transfer in patients with good prognosis.Crossref | GoogleScholarGoogle Scholar | 24893729PubMed |
Calin, G. A., Ferracin, M., Cimmino, A., Di Leva, G., Shimizu, M., Wojcik, S. E., Iorio, M. V., Visone, R., Sever, N. I., Fabbri, M., Iuliano, R., Palumbo, T., Pichiorri, F., Roldo, C., Garzon, R., Sevignani, C., Rassenti, L., Alder, H., Volinia, S., Liu, C. G., Kipps, T. J., Negrini, M., and Croce, C. M. (2005). A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353, 1793–1801.
| A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFKrtLbJ&md5=68645bd2ef133ebbaedd399e664e1604CAS | 16251535PubMed |
Carolan, C., Lonergan, P., Van Langendonckt, A., and Mermillod, P. (1995). Factors affecting bovine embryo development in synthetic oviduct fluid following oocyte maturation and fertilization in vitro. Theriogenology 43, 1115–1128.
| Factors affecting bovine embryo development in synthetic oviduct fluid following oocyte maturation and fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVCmtw%3D%3D&md5=d419e90c319ed0fd2da66dd599d7be0cCAS | 16727698PubMed |
Chim, S. S., Shing, T. K., Hung, E. C., Leung, T. Y., Lau, T. K., Chiu, R. W., and Lo, Y. M. (2008). Detection and characterization of placental microRNAs in maternal plasma. Clin. Chem. 54, 482–490.
| Detection and characterization of placental microRNAs in maternal plasma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivVansrc%3D&md5=fcc62624cced015d391f65b7ca239a66CAS | 18218722PubMed |
Chitwood, J. L., Rincon, G., Kaiser, G. G., Medrano, J. F., and Ross, P. J. (2013). RNA-seq analysis of single bovine blastocysts. BMC Genomics 14, 350.
| RNA-seq analysis of single bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpslyisrs%3D&md5=2ea4f7838c661e12e9005434bcd23162CAS | 23705625PubMed |
Cimmino, A., Calin, G. A., Fabbri, M., Iorio, M. V., Ferracin, M., Shimizu, M., Wojcik, S. E., Aqeilan, R. I., Zupo, S., Dono, M., Rassenti, L., Alder, H., Volinia, S., Liu, C. G., Kipps, T. J., Negrini, M., and Croce, C. M. (2005). miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl Acad. Sci. USA 102, 13 944–13 949.
| miR-15 and miR-16 induce apoptosis by targeting BCL2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOqsbjK&md5=8f2440059e32984662559ca3cabeb8d1CAS |
Cleys, E. R., Halleran, J. L., McWhorter, E., Hergenreder, J., Enriquez, V. A., da Silveira, J. C., Bruemmer, J. E., Winger, Q. A., and Bouma, G. J. (2014). Identification of microRNAs in exosomes isolated from serum and umbilical cord blood, as well as placentomes of gestational day 90 pregnant sheep. Mol. Reprod. Dev. 81, 983–993.
| Identification of microRNAs in exosomes isolated from serum and umbilical cord blood, as well as placentomes of gestational day 90 pregnant sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVykt77K&md5=93551972649180218a5206f31ddf6efdCAS | 25269776PubMed |
Coutinho, L. L., Matukumalli, L. K., Sonstegard, T. S., Van Tassell, C. P., Gasbarre, L. C., Capuco, A. V., and Smith, T. P. (2007). Discovery and profiling of bovine microRNAs from immune-related and embryonic tissues. Physiol. Genomics 29, 35–43.
| Discovery and profiling of bovine microRNAs from immune-related and embryonic tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVaru7s%3D&md5=1db55aa34732d3755236d4119413a17eCAS | 17105755PubMed |
Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. A. (2003). DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4, P3.
| DAVID: database for annotation, visualization, and integrated discovery.Crossref | GoogleScholarGoogle Scholar | 12734009PubMed |
Du, Y., Wang, X., Wang, B., Chen, W., He, R., Zhang, L., Xing, X., Su, J., Wang, Y., and Zhang, Y. (2014). Deep sequencing analysis of microRNAs in bovine sperm. Mol. Reprod. Dev. 81, 1042–1052.
| Deep sequencing analysis of microRNAs in bovine sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVykt7%2FN&md5=85e0a5400543da586a3867362422a291CAS | 25279827PubMed |
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. Sci. Rep. 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 | 1:CAS:528:DC%2BC2MXhtFKhtbvL&md5=539a46a23e392851fe75534c28bf1da4CAS | 25732513PubMed |
Fkih M’hamed, I., Privat, M., Ponelle, F., Penault-Llorca, F., Kenani, A., and Bignon, Y. J. (2015). Identification of miR-10b, miR-26a, miR-146a and miR-153 as potential triple-negative breast cancer biomarkers. Cell Oncol. (Dordr.) 38, 433–442.
| Identification of miR-10b, miR-26a, miR-146a and miR-153 as potential triple-negative breast cancer biomarkers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFyru77L&md5=46f93583f6113c05e007719b15ef05bfCAS | 26392359PubMed |
Fomeshi, M. R., Ebrahimi, M., Mowla, S. J., Khosravani, P., Firouzi, J., and Khayatzadeh, H. (2015). Evaluation of the expressions pattern of miR-10b, 21, 200c, 373 and 520c to find the correlation between epithelial-to-mesenchymal transition and melanoma stem cell potential in isolated cancer stem cells. Cell. Mol. Biol. Lett. 20, 448–465.
| Evaluation of the expressions pattern of miR-10b, 21, 200c, 373 and 520c to find the correlation between epithelial-to-mesenchymal transition and melanoma stem cell potential in isolated cancer stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1Ogu7jO&md5=d46323b9b41a8382fa738b381a9ea223CAS | 26208390PubMed |
Frankel, L. B., Christoffersen, N. R., Jacobsen, A., Lindow, M., Krogh, A., and Lund, A. H. (2008). Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J. Biol. Chem. 283, 1026–1033.
| Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFaktw%3D%3D&md5=25ce4b196351d23d6fea4533beb88383CAS | 17991735PubMed |
Friedländer, M. R., Mackowiak, S. D., Li, N., Chen, W., and Rajewsky, N. (2012). miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res. 40, 37–52.
| miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades.Crossref | GoogleScholarGoogle Scholar | 21911355PubMed |
Galli, C., Duchi, R., Colleoni, S., Lagutina, I., and Lazzari, G. (2014). Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice. Theriogenology 81, 138–151.
| Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice.Crossref | GoogleScholarGoogle Scholar | 24274418PubMed |
Galliano, D., and Pellicer, A. (2014). MicroRNA and implantation. Fertil. Steril. 101, 1531–1544.
| MicroRNA and implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvFGiurk%3D&md5=6526457026f47fea10e9c1c4ed8326d3CAS | 24882617PubMed |
Garzon, R., Volinia, S., Liu, C. G., Fernandez-Cymering, C., Palumbo, T., Pichiorri, F., Fabbri, M., Coombes, K., Alder, H., Nakamura, T., Flomenberg, N., Marcucci, G., Calin, G. A., Kornblau, S. M., Kantarjian, H., Bloomfield, C. D., Andreeff, M., and Croce, C. M. (2008a). MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood 111, 3183–3189.
| MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjvVamtbY%3D&md5=79ecb129fe97e5cb72b5081c7c7a0349CAS | 18187662PubMed |
Garzon, R., Garofalo, M., Martelli, M. P., Briesewitz, R., Wang, L., Fernandez-Cymering, C., Volinia, S., Liu, C. G., Schnittger, S., Haferlach, T., Liso, A., Diverio, D., Mancini, M., Meloni, G., Foa, R., Martelli, M. F., Mecucci, C., Croce, C. M., and Falini, B. (2008b). Distinctive miRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proc. Natl Acad. Sci. USA 105, 3945–3950.
| Distinctive miRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1OgtLw%3D&md5=ef555766f6d78b833a08caaf70bc751cCAS | 18308931PubMed |
Gebremedhn, S., Salilew-Wondim, D., Ahmad, I., Sahadevan, S., Hossain, M. M., Hoelker, M., Rings, F., Neuhoff, C., Tholen, E., Looft, C., Schellander, K., and Tesfaye, D. (2015). MicroRNA expression profile in bovine granulosa cells of preovulatory dominant and subordinate follicles during the late follicular phase of the estrous cycle. PLoS One 10, e0125912.
| MicroRNA expression profile in bovine granulosa cells of preovulatory dominant and subordinate follicles during the late follicular phase of the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 25993098PubMed |
Gilchrist, G. C., Tscherner, A., Nalpathamkalam, T., Merico, D., and LaMarre, J. (2016). MicroRNA expression during bovine oocyte maturation and fertilization. Int. J. Mol. Sci. 17, 396.
| MicroRNA expression during bovine oocyte maturation and fertilization.Crossref | GoogleScholarGoogle Scholar | 26999121PubMed |
Goossens, K., De Spiegelaere, W., Stevens, M., Burvenich, C., De Spiegeleer, B., Cornillie, P., Van Zeveren, A., Van Soom, A., and Peelman, L. (2012). Differential microRNA expression analysis in blastocysts by whole mount in situ hybridization and reverse transcription quantitative polymerase chain reaction on laser capture microdissection samples. Anal. Biochem. 423, 93–101.
| Differential microRNA expression analysis in blastocysts by whole mount in situ hybridization and reverse transcription quantitative polymerase chain reaction on laser capture microdissection samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsFOnu7o%3D&md5=b0b350c5afc3e6d7bb88b9a294dd71a1CAS | 22306474PubMed |
Goossens, K., Mestdagh, P., Lefever, S., Van Poucke, M., Van Zeveren, A., Van Soom, A., Vandesompele, J., and Peelman, L. (2013). Regulatory microRNA network identification in bovine blastocyst development. Stem Cells Dev. 22, 1907–1920.
| Regulatory microRNA network identification in bovine blastocyst development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpslCiu7Y%3D&md5=5ab005a937afe04daba24621d01c4bf3CAS | 23398486PubMed |
Goossens, K., Peelman, L., and Van Soom, A. (2014). MicroRNA in situ hybridization on whole-mount preimplantation embryos. Methods Mol. Biol. 1211, 15–25.
| MicroRNA in situ hybridization on whole-mount preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotlOhtr4%3D&md5=835fa92e9ca3e5d7f86ef3b9f8367ba8CAS | 25218373PubMed |
Imbar, T., Galliano, D., Pellicer, A., and Laufer, N. (2014). Introduction: MicroRNAs in human reproduction: small molecules with crucial regulatory roles. Fertil. Steril. 101, 1514–1515.
| Introduction: MicroRNAs in human reproduction: small molecules with crucial regulatory roles.Crossref | GoogleScholarGoogle Scholar | 24882615PubMed |
Jiang, J., and Hui, C. C. (2008). Hedgehog signaling in development and cancer. Dev. Cell 15, 801–812.
| Hedgehog signaling in development and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWgsbjN&md5=33b21c6d6f71d0089c16a3ead0bd2b05CAS | 19081070PubMed |
Jin, Y., Lu, J., Wen, J., Shen, Y., and Wen, X. (2015). Regulation of growth of human bladder cancer by miR-192. Tumour Biol. 36, 3791–3797.
| Regulation of growth of human bladder cancer by miR-192.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVCrtL4%3D&md5=a648d55f5ae2a79c19c87d8fd212d99eCAS | 25566965PubMed |
Kambe, S., Yoshitake, H., Yuge, K., Ishida, Y., Ali, M. M., Takizawa, T., Kuwata, T., Ohkuchi, A., Matsubara, S., Suzuki, M., Takeshita, T., Saito, S., and Takizawa, T. (2014). Human exosomal placenta-associated miR-517a-3p modulates the expression of PRKG1 mRNA in Jurkat cells. Biol. Reprod. 91, 129.
| Human exosomal placenta-associated miR-517a-3p modulates the expression of PRKG1 mRNA in Jurkat cells.Crossref | GoogleScholarGoogle Scholar | 25273530PubMed |
Kang, J. T., Atikuzzaman, M., Kwon, D. K., Park, S. J., Kim, S. J., Moon, J. H., Koo, O. J., Jang, G., and Lee, B. C. (2012). Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations. Zygote 20, 1–8.
| Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1arug%3D%3D&md5=57ce80ab1a5e168d7f9c34ca1c783e0aCAS | 21791162PubMed |
Kang, Y. J., Lees, M., Matthews, L. C., Kimber, S. J., Forbes, K., and Aplin, J. D. (2015). MiR-145 suppresses embryo–epithelial juxtacrine communication at implantation by modulating maternal IGF1R. J. Cell Sci. 128, 804–814.
| MiR-145 suppresses embryo–epithelial juxtacrine communication at implantation by modulating maternal IGF1R.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmtlSitr8%3D&md5=abfa3d86ddeac109450ef1306fa72f24CAS | 25609710PubMed |
Karube, Y., Tanaka, H., Osada, H., Tomida, S., Tatematsu, Y., Yanagisawa, K., Yatabe, Y., Takamizawa, J., Miyoshi, S., Mitsudomi, T., and Takahashi, T. (2005). Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci. 96, 111–115.
| Reduced expression of Dicer associated with poor prognosis in lung cancer patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislOhs7g%3D&md5=5dcadd6dcf5f21e228d75ca6217e439fCAS | 15723655PubMed |
Kozomara, A., and Griffiths-Jones, S. (2014). miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42, D68–D73.
| miRBase: annotating high confidence microRNAs using deep sequencing data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXos1Wk&md5=7391794021fb3c9fa2fc8c2431316780CAS | 24275495PubMed |
Kridli, R. T., Khalaj, K., Bidarimath, M., and Tayade, C. (2016). Placentation, maternal–fetal interface, and conceptus loss in swine. Theriogenology 85, .
| Placentation, maternal–fetal interface, and conceptus loss in swine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlOmt7jP&md5=f1228a77188c8e6b2ec65bc4bb3fc9aeCAS | 26324112PubMed |
Kropp, J., and Khatib, H. (2015). Characterization of microRNA in bovine in vitro culture media associated with embryo quality and development. J. Dairy Sci. 98, 6552–6563.
| Characterization of microRNA in bovine in vitro culture media associated with embryo quality and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFehsL7P&md5=8ba33dce67938c37af37c51541d4d11bCAS | 26142856PubMed |
Kropp, J., Salih, S. M., and Khatib, H. (2014). Expression of microRNAs in bovine and human pre-implantation embryo culture media. Front. Genet. 5, 91.
| Expression of microRNAs in bovine and human pre-implantation embryo culture media.Crossref | GoogleScholarGoogle Scholar | 24795753PubMed |
Li, G., Cai, M., Fu, D., Chen, K., Sun, M., Cai, Z., and Cheng, B. (2012). Heat shock protein 90B1 plays an oncogenic role and is a target of microRNA-223 in human osteosarcoma. Cell. Physiol. Biochem. 30, 1481–1490.
| Heat shock protein 90B1 plays an oncogenic role and is a target of microRNA-223 in human osteosarcoma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslWitrk%3D&md5=d68ec7892061a98a4bac6107782475a8CAS | 23208072PubMed |
Li, Y., Fang, Y., Liu, Y., and Yang, X. (2015a). MicroRNAs in ovarian function and disorders. J. Ovarian Res. 8, 51.
| MicroRNAs in ovarian function and disorders.Crossref | GoogleScholarGoogle Scholar | 26232057PubMed |
Li, Z., Jia, J., Gou, J., Tong, A., Liu, X., Zhao, X., and Yi, T. (2015b). Mmu-miR-126a-3p plays a role in murine embryo implantation by regulating Itga11. Reprod. Biomed. Online 31, 384–393.
| Mmu-miR-126a-3p plays a role in murine embryo implantation by regulating Itga11.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVeksLvK&md5=48e161c1a6225bfac8f3dc157538f3e0CAS | 26194885PubMed |
Liang, X., Liu, Y., Mei, S., Zhang, M., Xin, J., Zhang, Y., and Yang, R. (2015). MicroRNA-22 impairs anti-tumor ability of dendritic cells by targeting p38. PLoS One 10, e0121510.
| MicroRNA-22 impairs anti-tumor ability of dendritic cells by targeting p38.Crossref | GoogleScholarGoogle Scholar | 25826372PubMed |
Marzi, M. J., Puggioni, E. M., Dall’Olio, V., Bucci, G., Bernard, L., Bianchi, F., Crescenzi, M., Di Fiore, P. P., and Nicassio, F. (2012). Differentiation-associated microRNAs antagonize the Rb-E2F pathway to restrict proliferation. J. Cell Biol. 199, 77–95.
| Differentiation-associated microRNAs antagonize the Rb-E2F pathway to restrict proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsV2it73M&md5=693ce7e2c769fd5d944f0e0f1fd80df1CAS | 23027903PubMed |
McCallie, B. R., Parks, J. C., Strieby, A. L., Schoolcraft, W. B., and Katz-Jaffe, M. G. (2014). Human blastocysts exhibit unique microrna profiles in relation to maternal age and chromosome constitution. J. Assist. Reprod. Genet. 31, 913–919.
| Human blastocysts exhibit unique microrna profiles in relation to maternal age and chromosome constitution.Crossref | GoogleScholarGoogle Scholar | 24760722PubMed |
McManus, M. T. (2003). MicroRNAs and cancer. Semin. Cancer Biol. 13, 253–258.
| MicroRNAs and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFykurY%3D&md5=b6b53dd67ac0e27b2fc3fb2f025beaa1CAS | 14563119PubMed |
Mitchell, M. D., Peiris, H. N., Kobayashi, M., Koh, Y. Q., Duncombe, G., Illanes, S. E., Rice, G. E., and Salomon, C. (2015). Placental exosomes in normal and complicated pregnancy. Am. J. Obstet. Gynecol. 213, S173–S181.
| Placental exosomes in normal and complicated pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvFygtL8%3D&md5=cf2aee773795b546807123d3e073d559CAS | 26428497PubMed |
Mondou, E., Dufort, I., Gohin, M., Fournier, E., and Sirard, M. A. (2012). Analysis of microRNAs and their precursors in bovine early embryonic development. Mol. Hum. Reprod. 18, 425–434.
| Analysis of microRNAs and their precursors in bovine early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlWmur3L&md5=e86b0dfd9006ee489f2c4ec366f4159dCAS | 22491901PubMed |
Monk, M., and Holding, C. (2001). Human embryonic genes re-expressed in cancer cells. Oncogene 20, 8085–8091.
| Human embryonic genes re-expressed in cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptlKktb8%3D&md5=e359d7f4fde42d2fa66ca74f37ab4e2eCAS | 11781821PubMed |
Murri, M., Insenser, M., Fernández-Durán, E., San-Millán, J. L., and Escobar-Morreale, H. F. (2013). Effects of polycystic ovary syndrome (PCOS), sex hormones, and obesity on circulating miRNA-21, miRNA-27b, miRNA-103, and miRNA-155 expression. J. Clin. Endocrinol. Metab. 98, E1835–E1844.
| Effects of polycystic ovary syndrome (PCOS), sex hormones, and obesity on circulating miRNA-21, miRNA-27b, miRNA-103, and miRNA-155 expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsl2msrjL&md5=3d18e0106c379052c1a6f61b78507abfCAS | 24037889PubMed |
Nagaraj, N. S., and Datta, P. K. (2010). Targeting the transforming growth factor-beta signaling pathway in human cancer. Expert Opin. Investig. Drugs 19, 77–91.
| Targeting the transforming growth factor-beta signaling pathway in human cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFCiu77J&md5=f9a25042c24b6e5f16a2bdbbd2fc59cfCAS | 20001556PubMed |
Nagpal, N., Ahmad, H. M., Chameettachal, S., Sundar, D., Ghosh, S., and Kulshreshtha, R. (2015). HIF-inducible miR-191 promotes migration in breast cancer through complex regulation of TGFβ-signaling in hypoxic microenvironment. Sci. Rep. 5, 9650.
| HIF-inducible miR-191 promotes migration in breast cancer through complex regulation of TGFβ-signaling in hypoxic microenvironment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFOrsrnL&md5=e8ca24659d2495ee082fcdc00e418d30CAS | 25867965PubMed |
Nishida, N., Nagahara, M., Sato, T., Mimori, K., Sudo, T., Tanaka, F., Shibata, K., Ishii, H., Sugihara, K., Doki, Y., and Mori, M. (2012). Microarray analysis of colorectal cancer stromal tissue reveals upregulation of two oncogenic miRNA clusters. Clin. Cancer Res. 18, 3054–3070.
| Microarray analysis of colorectal cancer stromal tissue reveals upregulation of two oncogenic miRNA clusters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvVOgtLY%3D&md5=e59ecab15f17520fdd102dea750109b8CAS | 22452939PubMed |
Nishioka, N., Inoue, K., Adachi, K., Kiyonari, H., Ota, M., Ralston, A., Yabuta, N., Hirahara, S., Stephenson, R. O., Ogonuki, N., Makita, R., Kurihara, H., Morin-Kensicki, E. M., Nojima, H., Rossant, J., Nakao, K., Niwa, H., and Sasaki, H. (2009). The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16, 398–410.
| The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjs1ynsrw%3D&md5=9c7f38d72431e6e12aefecae8bdc6d1eCAS | 19289085PubMed |
O’Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V., and Mendell, J. T. (2005). c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839–843.
| c-Myc-regulated microRNAs modulate E2F1 expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVGgsLg%3D&md5=9cb95b56cdfdb05e57e8b00cd4fe3a38CAS | 15944709PubMed |
O’Hara, L., Forde, N., Kelly, A. K., and Lonergan, P. (2014). Effect of bovine blastocyst size at embryo transfer on Day 7 on conceptus length on Day 14: can supplementary progesterone rescue small embryos? Theriogenology 81, 1123–1128.
| Effect of bovine blastocyst size at embryo transfer on Day 7 on conceptus length on Day 14: can supplementary progesterone rescue small embryos?Crossref | GoogleScholarGoogle Scholar | 24582375PubMed |
Palacios, F., Abreu, C., Prieto, D., Morande, P., Ruiz, S., Fernández-Calero, T., Naya, H., Libisch, G., Robello, C., Landoni, A. I., Gabus, R., Dighiero, G., and Oppezzo, P. (2015). Activation of the PI3K/AKT pathway by microRNA-22 results in CLL B-cell proliferation. Leukemia 29, 115–125.
| Activation of the PI3K/AKT pathway by microRNA-22 results in CLL B-cell proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpsFekt7o%3D&md5=7fab101c64dc9e30a72c9feb6f8d42a9CAS | 24825182PubMed |
Pan, B., Toms, D., Shen, W., and Li, J. (2015). MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells. Am. J. Physiol. Endocrinol. Metab. 308, E525–E534.
| MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXls1CrtLY%3D&md5=a5426fd7e0de22a29e48fd888276bac1CAS | 25628423PubMed |
Pasqualini, L., Bu, H., Puhr, M., Narisu, N., Rainer, J., Schlick, B., Schäfer, G., Angelova, M., Trajanoski, Z., Börno, S. T., Schweiger, M. R., Fuchsberger, C., and Klocker, H. (2015). miR-22 and miR-29a are members of the androgen receptor cistrome modulating LAMC1 and Mcl-1 in prostate cancer. Mol. Endocrinol. 29, 1037–1054.
| miR-22 and miR-29a are members of the androgen receptor cistrome modulating LAMC1 and Mcl-1 in prostate cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFykurrP&md5=df15239bc05f2f76e1fa9424cce31110CAS | 26052614PubMed |
Petrocca, F., Visone, R., Onelli, M. R., Shah, M. H., Nicoloso, M. S., de Martino, I., Iliopoulos, D., Pilozzi, E., Liu, C. G., Negrini, M., Cavazzini, L., Volinia, S., Alder, H., Ruco, L. P., Baldassarre, G., Croce, C. M., and Vecchione, A. (2008). E2F1-regulated microRNAs impair TGFβ-dependent cell cycle arrest and apoptosis in gastric cancer. Cancer Cell 13, 272–286.
| E2F1-regulated microRNAs impair TGFβ-dependent cell cycle arrest and apoptosis in gastric cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVKgs7s%3D&md5=fa3c22f7dfb11d1ecc152cb5d0dc50feCAS | 18328430PubMed |
Ponsuksili, S., Tesfaye, D., Schellander, K., Hoelker, M., Hadlich, F., Schwerin, M., and Wimmers, K. (2014). Differential expression of miRNAs and their target mRNAs in endometria prior to maternal recognition of pregnancy associates with endometrial receptivity for in vivo- and in vitro-produced bovine embryos. Biol. Reprod. 91, 135.
| Differential expression of miRNAs and their target mRNAs in endometria prior to maternal recognition of pregnancy associates with endometrial receptivity for in vivo- and in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 25253731PubMed |
Rayner, K. J., and Hennessy, E. J. (2013). Extracellular communication via microRNA: lipid particles have a new message. J. Lipid Res. 54, 1174–1181.
| Extracellular communication via microRNA: lipid particles have a new message.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsFeksLg%3D&md5=e2dc059ddd8898c5c314fd74c4e9e07eCAS | 23505318PubMed |
Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–248.
| Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Giug%3D%3D&md5=fd530554a4e416cc604ed66ebc4922a4CAS | 11803560PubMed |
Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.
| edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WlurvO&md5=f460abb200a8b720c3960b07d113133cCAS | 19910308PubMed |
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 | 1:CAS:528:DC%2BC2cXksFWgurs%3D&md5=2ebfae343916492955cea19747f52860CAS | 24786747PubMed |
Salilew-Wondim, D., Ahmad, I., Gebremedhn, S., Sahadevan, S., Hossain, M. D., Rings, F., Hoelker, M., Tholen, E., Neuhoff, C., Looft, C., Schellander, K., and Tesfaye, D. (2014). The expression pattern of microRNAs in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle. PLoS One 9, e106795.
| The expression pattern of microRNAs in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle.Crossref | GoogleScholarGoogle Scholar | 25192015PubMed |
Sohel, M. M., Hoelker, M., Noferesti, S. S., Salilew-Wondim, D., Tholen, E., Looft, C., Rings, F., Uddin, M. J., Spencer, T. E., Schellander, K., and Tesfaye, D. (2013). Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One 8, e78505.
| Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGisLjJ&md5=48d1c73f7d3de8b6134d507fb2898365CAS | 24223816PubMed |
Song, L., Liu, L., Wu, Z., Li, Y., Ying, Z., Lin, C., Wu, J., Hu, B., Cheng, S. Y., Li, M., and Li, J. (2012). TGF-β induces miR-182 to sustain NF-κB activation in glioma subsets. J. Clin. Invest. 122, 3563–3578.
| TGF-β induces miR-182 to sustain NF-κB activation in glioma subsets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsV2itrfF&md5=43c3e83da0698a7d0e82b6c6aac796e2CAS | 23006329PubMed |
Song, J. L., Nigam, P., Tektas, S. S., and Selva, E. (2015). microRNA regulation of Wnt signaling pathways in development and disease. Cell. Signal. 27, 1380–1391.
| microRNA regulation of Wnt signaling pathways in development and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmsF2hurw%3D&md5=d96dccfdb180a7df6c8790ce93ed4913CAS | 25843779PubMed |
Stowe, H. M., Calcatera, S. M., Dimmick, M. A., Andrae, J. G., Duckett, S. K., and Pratt, S. L. (2014). The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression. PLoS One 9, e113163.
| The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression.Crossref | GoogleScholarGoogle Scholar | 25462855PubMed |
Su, J., Liu, X., Sun, H., Wang, Y., Wu, Y., Guo, Z., and Zhang, Y. (2015). Identification of differentially expressed microRNAs in placentas of cloned and normally produced calves by Solexa sequencing. Anim. Reprod. Sci. 155, 64–74.
| Identification of differentially expressed microRNAs in placentas of cloned and normally produced calves by Solexa sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXivFGqsLw%3D&md5=1c15e6c947fa0b103eb6a329ddb68281CAS | 25735829PubMed |
Toms, D., Xu, S., Pan, B., Wu, D., and Li, J. (2015). Progesterone receptor expression in granulosa cells is suppressed by microRNA-378-3p. Mol. Cell. Endocrinol. 399, 95–102.
| Progesterone receptor expression in granulosa cells is suppressed by microRNA-378-3p.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVKntLfP&md5=0fd6d50aa42201b6f5941ce5d0eb531dCAS | 25150622PubMed |
Tripurani, S. K., Xiao, C., Salem, M., and Yao, J. (2010). Cloning and analysis of fetal ovary microRNAs in cattle. Anim. Reprod. Sci. 120, 16–22.
| Cloning and analysis of fetal ovary microRNAs in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFWrtr0%3D&md5=51f45ec6d2550f1c7e8e90778cd6ca8fCAS | 20347535PubMed |
Tscherner, A., Gilchrist, G., Smith, N., Blondin, P., Gillis, D., and LaMarre, J. (2014). MicroRNA-34 family expression in bovine gametes and preimplantation embryos. Reprod. Biol. Endocrinol. 12, 85.
| MicroRNA-34 family expression in bovine gametes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 25179211PubMed |
Vlachos, I. S., Kostoulas, N., Vergoulis, T., Georgakilas, G., Reczko, M., Maragkakis, M., Paraskevopoulou, M. D., Prionidis, K., Dalamagas, T., and Hatzigeorgiou, A. G. (2012). DIANA miRPath v.2.0: investigating the combinatorial effect of microRNAs in pathways. Nucleic Acids Res. 40, W498–W504.
| DIANA miRPath v.2.0: investigating the combinatorial effect of microRNAs in pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtVCqs7Y%3D&md5=25651ee16204e8206ef441f7fac32ed7CAS | 22649059PubMed |
Volinia, S., Calin, G., Liu, C. G., Ambs, S., Cimmino, A., Petrocca, F., Visone, R., Iorio, M., Roldo, C., Ferracin, M., Prueitt, R. L., Yanaihara, N., Lanza, G., Scarpa, A., Vecchione, A., Negrini, M., Harris, C. C., and Croce, C. M. (2006). A microRNA expression signature in human solid tumors defines cancer targets. Proc. Natl Acad. Sci. USA 103, 2257–2261.
| A microRNA expression signature in human solid tumors defines cancer targets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhslGjsbg%3D&md5=5fc897d482e4d21db86be48e8eadc17eCAS | 16461460PubMed |
Voorhoeve, P. M., le Sage, C., Schrier, M., Gillis, A. J., Stoop, H., Nagel, R., Liu, Y. P., van Duijse, J., Drost, J., Griekspoor, A., Zlotorynski, E., Yabuta, N., De Vita, G., Nojima, H., Looijenga, L. H., and Agami, R. (2006). A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124, 1169–1181.
| A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1Khsrg%3D&md5=93af690f0133b5c64804f2265818a8fcCAS | 16564011PubMed |
Wydooghe, E., Vandaele, L., Heras, S., De Sutter, P., Deforce, D., Peelman, L., De Schauwer, C., and Van Soom, A. (2015). Autocrine embryotropins revisited: how do embryos communicate with each other in vitro when cultured in groups? Biol. Rev. Camb. Philos. Soc. , .
| Autocrine embryotropins revisited: how do embryos communicate with each other in vitro when cultured in groups?Crossref | GoogleScholarGoogle Scholar | 26608222PubMed |
Xu, D., Takeshita, F., Hino, Y., Fukunaga, S., Kudo, Y., Tamakim, A., Matsunaga, J., Takahashi, R. U., Takata, T., Shimamoto, A., Ochiya, T., and Tahara, H. (2011). miR-22 represses cancer progression by inducing cellular senescence. J. Cell Biol. 193, 409–424.
| miR-22 represses cancer progression by inducing cellular senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGjt7o%3D&md5=1b9b50d2e937a61f47dde6e17a5b3b9cCAS | 21502362PubMed |
Xue, J., Chen, Z., Gu, X., Zhang, Y., and Zhang, W. (2016). MicroRNA-148a inhibits migration of breast cancer cells by targeting MMP-13. Tumour Biol. 37, 1581–1590.
| MicroRNA-148a inhibits migration of breast cancer cells by targeting MMP-13.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVWgsbfJ&md5=df26770cf0fd3607e45c499ab31c9611CAS | 26298724PubMed |
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. Dev. Dyn. 237, 2315–2327.
| Determination of microRNAs in mouse preimplantation embryos by microarray.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFylsb%2FF&md5=53bf0631d9c29423f71d2a3cced85a59CAS | 18729214PubMed |
