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RESEARCH ARTICLE
Contents Vol 27(1)

Exploring the function of long non-coding RNA in the development of bovine early embryos

Julieta Caballero A , Isabelle Gilbert A , Eric Fournier A , Dominic Gagné A , Sara Scantland A , Angus Macaulay A and Claude Robert A B
+ Author Affiliations
- Author Affiliations

A Département des sciences animales, Centre de recherche en biologie de la reproduction, Institut sur la nutrition et les aliments fonctionnels, Université Laval, 2440 boulevard Hochelaga QC, G1V 0A6, Canada.

B Corresponding author. Email: claude.robert@fsaa.ulaval.ca

Reproduction, Fertility and Development 27(1) 40-52 https://doi.org/10.1071/RD14338
Published: 4 December 2014

Abstract

Now recognised as part of the cellular transcriptome, the function of long non-coding (lnc) RNA remains unclear. Previously, we found that some lncRNA molecules in bovine embryos are highly responsive to culture conditions. In view of a recent demonstration that lncRNA may play a role in regulating important functions, such as maintenance of pluripotency, modification of epigenetic marks and activation of transcription, we sought evidence of its involvement in embryogenesis. Among the numerous catalogued lncRNA molecules found in oocytes and early embryos of cattle, three candidates chosen for further characterisation were found unexpectedly in the cytoplasmic compartment rather than in the nucleus. Transcriptomic survey of subcellular fractions found these candidates also associated with polyribosomes and one of them spanning transzonal projections between cumulus cells and the oocyte. Knocking down this transcript in matured oocytes increased developmental rates, leading to larger blastocysts. Transcriptome and methylome analyses of these blastocysts showed concordant data for a subset of four genes, including at least one known to be important for blastocyst survival. Functional characterisation of the roles played by lncRNA in supporting early development remains elusive. Our results suggest that some lncRNAs play a role in translation control of target mRNA. This would be important for managing the maternal reserves within which is embedded the embryonic program, especially before embryonic genome activation.

Additional keywords: cytoplasm, knockdown, methylome, polyribosome, transcriptome, transzonal projection.


References

Bai, Q., Assou, S., Haouzi, D., Ramirez, J. M., Monzo, C., Becker, F., Gerbal-Chaloin, S., Hamamah, S., and De Vos, J. (2012). Dissecting the first transcriptional divergence during human embryonic development. Stem Cell Rev. 8, 150–162.
| Dissecting the first transcriptional divergence during human embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtVCru70%3D&md5=724710b27bcfc99909ed935f167e6c0fCAS | 21750961PubMed |

Bánfai, B., Jia, H., Khatun, J., Wood, E., Risk, B., Gundling, W. E., Kundaje, A., Gunawardena, H. P., Yu, Y., Xie, L., Krajewski, K., Strahl, B. D., Chen, X., Bickel, P., Giddings, M. C., Brown, J. B., and Lipovich, L. (2012). Long noncoding RNAs are rarely translated in two human cell lines. Genome Res. 22, 1646–1657.
| Long noncoding RNAs are rarely translated in two human cell lines.Crossref | GoogleScholarGoogle Scholar | 22955977PubMed |

Bianco, C., Normanno, N., Salomon, D. S., and Ciardiello, F. (2004). Role of the cripto (EGF-CFC) family in embryogenesis and cancer. Growth Factors 22, 133–139.
| Role of the cripto (EGF-CFC) family in embryogenesis and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1aksr4%3D&md5=a98259c6976d9e313e8fc02bdf777323CAS | 15518236PubMed |

Brockdorff, N., Ashworth, A., Kay, G. F., Cooper, P., Smith, S., McCabe, V. M., Norris, D. P., Penny, G. D., Patel, D., and Rastan, S. (1991). Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 351, 329–331.
| Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1Grurw%3D&md5=8c17de9ed671e587c09de899ad6acbe4CAS | 2034279PubMed |

Bui, L. C., Evsikov, A. V., Khan, D. R., Archilla, C., Peynot, N., Henaut, A., Le Bourhis, D., Vignon, X., Renard, J. P., and Duranthon, V. (2009). Retrotransposon expression as a defining event of genome reprogramming in fertilized and cloned bovine embryos. Reproduction 138, 289–299.
| Retrotransposon expression as a defining event of genome reprogramming in fertilized and cloned bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptlemt7Y%3D&md5=4512f7f91433160c2f0c40f23fd41097CAS | 19465487PubMed |

Caballero, J. N., Frenette, G., Belleannee, C., and Sullivan, R. (2013). CD9-positive microvesicles mediate the transfer of molecules to bovine spermatozoa during epididymal maturation. PLoS ONE 8, e65364.
| CD9-positive microvesicles mediate the transfer of molecules to bovine spermatozoa during epididymal maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVejtrrJ&md5=98be7f977cd3a4b5f77a37d647d7427eCAS | 23785420PubMed |

Carrieri, C., Cimatti, L., Biagioli, M., Beugnet, A., Zucchelli, S., Fedele, S., Pesce, E., Ferrer, I., Collavin, L., Santoro, C., Forrest, A. R., Carninci, P., Biffo, S., Stupka, E., and Gustincich, S. (2012). Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491, 454–457.
| Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsV2rsLbM&md5=9ac2445c7a3f7d3c9a676fef55f0dd91CAS | 23064229PubMed |

Clemson, C. M., Hutchinson, J. N., Sara, S. A., Ensminger, A. W., Fox, A. H., Chess, A., and Lawrence, J. B. (2009). An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell 33, 717–726.
| An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFSmsL4%3D&md5=0b0027543868dfb95488187dc1b743b1CAS | 19217333PubMed |

Cordaux, R., and Batzer, M. A. (2009). The impact of retrotransposons on human genome evolution. Nat. Rev. Genet. 10, 691–703.
| The impact of retrotransposons on human genome evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFCqurjM&md5=3979bb6fee38e8110e72470a378be423CAS | 19763152PubMed |

Côté, I., Vigneault, C., Laflamme, I., Laquerre, J., Fournier, E., Gilbert, I., Scantland, S., Gagné, D., Blondin, P., and Robert, C. (2011). Comprehensive cross production system assessment of the impact of in vitro microenvironment on the expression of messengers and long non-coding RNAs in the bovine blastocyst. Reproduction 142, 99–112.
| Comprehensive cross production system assessment of the impact of in vitro microenvironment on the expression of messengers and long non-coding RNAs in the bovine blastocyst.Crossref | GoogleScholarGoogle Scholar | 21487002PubMed |

Derrien, T., Johnson, R., Bussotti, G., Tanzer, A., Djebali, S., Tilgner, H., Guernec, G., Martin, D., Merkel, A., Knowles, D. G., Lagarde, J., Veeravalli, L., Ruan, X., Ruan, Y., Lassmann, T., Carninci, P., Brown, J. B., Lipovich, L., Gonzalez, J. M., Thomas, M., Davis, C. A., Shiekhattar, R., Gingeras, T. R., Hubbard, T. J., Notredame, C., Harrow, J., and Guigo, R. (2012). The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 22, 1775–1789.
| The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlentLvO&md5=8a0e23d89af76ebc961e419177cd7640CAS | 22955988PubMed |

Dinger, M. E., Amaral, P. P., Mercer, T. R., Pang, K. C., Bruce, S. J., Gardiner, B. B., Askarian-Amiri, M. E., Ru, K., Solda, G., Simons, C., Sunkin, S. M., Crowe, M. L., Grimmond, S. M., Perkins, A. C., and Mattick, J. S. (2008). Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 18, 1433–1445.
| Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtV2qsr3N&md5=b18f4d11ccc2771ae3b0dd0be3f03f0dCAS | 18562676PubMed |

Djebali, S., Davis, C. A., Merkel, A., Dobin, A., Lassmann, T., Mortazavi, A., Tanzer, A., Lagarde, J., Lin, W., Schlesinger, F., Xue, C., Marinov, G. K., Khatun, J., Williams, B. A., Zaleski, C., Rozowsky, J., Roder, M., Kokocinski, F., Abdelhamid, R. F., Alioto, T., Antoshechkin, I., Baer, M. T., Bar, N. S., Batut, P., Bell, K., Bell, I., Chakrabortty, S., Chen, X., Chrast, J., Curado, J., Derrien, T., Drenkow, J., Dumais, E., Dumais, J., Duttagupta, R., Falconnet, E., Fastuca, M., Fejes-Toth, K., Ferreira, P., Foissac, S., Fullwood, M. J., Gao, H., Gonzalez, D., Gordon, A., Gunawardena, H., Howald, C., Jha, S., Johnson, R., Kapranov, P., King, B., Kingswood, C., Luo, O. J., Park, E., Persaud, K., Preall, J. B., Ribeca, P., Risk, B., Robyr, D., Sammeth, M., Schaffer, L., See, L. H., Shahab, A., Skancke, J., Suzuki, A. M., Takahashi, H., Tilgner, H., Trout, D., Walters, N., Wang, H., Wrobel, J., Yu, Y., Ruan, X., Hayashizaki, Y., Harrow, J., Gerstein, M., Hubbard, T., Reymond, A., Antonarakis, S. E., Hannon, G., Giddings, M. C., Ruan, Y., Wold, B., Carninci, P., Guigo, R., and Gingeras, T. R. (2012). Landscape of transcription in human cells. Nature 489, 101–108.
| Landscape of transcription in human cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGnt73M&md5=46febdd3c069a9b5975a0c00637489afCAS | 22955620PubMed |

El-Sayed, A., Hoelker, M., Rings, F., Salilew, D., Jennen, D., Tholen, E., Sirard, M. A., Schellander, K., and Tesfaye, D. (2006). Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiol. Genomics 28, 84–96.
| Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCmtrzK&md5=d361eae34c584da7082823e33be5d6dbCAS | 17018689PubMed |

Excoffon, K. J., Avenarius, M. R., Hansen, M. R., Kimberling, W. J., Najmabadi, H., Smith, R. J., and Zabner, J. (2006). The Coxsackievirus and adenovirus receptor: a new adhesion protein in cochlear development. Hear. Res. 215, 1–9.
| The Coxsackievirus and adenovirus receptor: a new adhesion protein in cochlear development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVCqsL0%3D&md5=9b541af0789ff2993ed00908d15231fbCAS | 16678988PubMed |

Gong, C., Popp, M. W., and Maquat, L. E. (2012). Biochemical analysis of long non-coding RNA-containing ribonucleoprotein complexes. Methods 58, 88–93.
| Biochemical analysis of long non-coding RNA-containing ribonucleoprotein complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFGisLjI&md5=dfcb361dffa389c1eda693e7f8bfddccCAS | 22789663PubMed |

Guttman, M., Amit, I., Garber, M., French, C., Lin, M. F., Feldser, D., Huarte, M., Zuk, O., Carey, B. W., Cassady, J. P., Cabili, M. N., Jaenisch, R., Mikkelsen, T. S., Jacks, T., Hacohen, N., Bernstein, B. E., Kellis, M., Regev, A., Rinn, J. L., and Lander, E. S. (2009). Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223–227.
| Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1ehsbo%3D&md5=8e46055006ae1cb770a1a4d36b0be9bcCAS | 19182780PubMed |

Guttman, M., Garber, M., Levin, J. Z., Donaghey, J., Robinson, J., Adiconis, X., Fan, L., Koziol, M. J., Gnirke, A., Nusbaum, C., Rinn, J. L., Lander, E. S., and Regev, A. (2010). Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat. Biotechnol. 28, 503–510.
| Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVyitbs%3D&md5=54cf1c766e26aefe77a6e36e6b1cb066CAS | 20436462PubMed |

Guttman, M., Russell, P., Ingolia, N. T., Weissman, J. S., and Lander, E. S. (2013). Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154, 240–251.
| Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVehsLbF&md5=d8a41ed9ad7d6b0cde271921240ea9c3CAS | 23810193PubMed |

Hangauer, M. J., Vaughn, I. W., and McManus, M. T. (2013). Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet. 9, e1003569.
| Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFersLvL&md5=370ac0c05ad94f9348692ebcbf5dc25aCAS | 23818866PubMed |

Hemler, M. E. (2005). Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6, 801–811.
| Tetraspanin functions and associated microdomains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFertbrK&md5=4d09b0011695ecc6794fc3ee908cf7dcCAS | 16314869PubMed |

Huang, Y., Liu, N., Wang, J. P., Wang, Y. Q., Yu, X. L., Wang, Z. B., Cheng, X. C., and Zou, Q. (2012). Regulatory long non-coding RNA and its functions. J. Physiol. Biochem. 68, 611–618.
| Regulatory long non-coding RNA and its functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslWrurnF&md5=0ec44b14ccac4bd1800bee157a47b3ebCAS | 22535282PubMed |

Ingolia, N. T., Brar, G. A., Rouskin, S., McGeachy, A. M., and Weissman, J. S. (2013). Genome-wide annotation and quantitation of translation by ribosome profiling. In ‘Current Protocols in Molecular Biology’.10.1002/0471142727.MB0418S103

Jégou, A., Ziyyat, A., Barraud-Lange, V., Perez, E., Wolf, J. P., Pincet, F., and Gourier, C. (2011). CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization. Proc. Natl Acad. Sci. USA 108, 10 946–10 951.
| CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization.Crossref | GoogleScholarGoogle Scholar |

Jia, H., Osak, M., Bogu, G. K., Stanton, L. W., Johnson, R., and Lipovich, L. (2010). Genome-wide computational identification and manual annotation of human long noncoding RNA genes. RNA 16, 1478–1487.
| Genome-wide computational identification and manual annotation of human long noncoding RNA genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVCltLzL&md5=68a16bf14203fece5223e2b39fbdb8f4CAS | 20587619PubMed |

Kimber, S. J., Sneddon, S. F., Bloor, D. J., El-Bareg, A. M., Hawkhead, J. A., Metcalfe, A. D., Houghton, F. D., Leese, H. J., Rutherford, A., Lieberman, B. A., and Brison, D. R. (2008). Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors. Reproduction 135, 635–647.
| Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1Wqur4%3D&md5=48f29b65c3d7fe18ed4d180ea5ab2ec5CAS | 18411410PubMed |

Lapidot, M., and Pilpel, Y. (2006). Genome-wide natural antisense transcription: coupling its regulation to its different regulatory mechanisms. EMBO Rep. 7, 1216–1222.
| Genome-wide natural antisense transcription: coupling its regulation to its different regulatory mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Kju7zN&md5=e402efff1f4f1883e818288c8a48a9adCAS | 17139297PubMed |

Li, L., and Chang, H. Y. (2014). Physiological roles of long noncoding RNAs: insight from knockout mice. Trends Cell Biol. , .
| Physiological roles of long noncoding RNAs: insight from knockout mice.Crossref | GoogleScholarGoogle Scholar | 25022466PubMed |

Loewer, S., Cabili, M. N., Guttman, M., Loh, Y. H., Thomas, K., Park, I. H., Garber, M., Curran, M., Onder, T., Agarwal, S., Manos, P. D., Datta, S., Lander, E. S., Schlaeger, T. M., Daley, G. Q., and Rinn, J. L. (2010). Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat. Genet. 42, 1113–1117.
| Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2jsbzE&md5=eac3a407e825252791525f8990de600eCAS | 21057500PubMed |

Macaulay, A. D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., Sirard, M. A., Clarke, H. J., Khandjian, E. W., Richard, F. J., Hyttel, P., and Robert, R. (2014). The gametic synapse; RNA transfer to the oocyte. Biol. Reprod. , .
| The gametic synapse; RNA transfer to the oocyte.Crossref | GoogleScholarGoogle Scholar | 25143353PubMed |

Marks, P. W., Arai, M., Bandura, J. L., and Kwiatkowski, D. J. (1998). Advillin (p92): a new member of the gelsolin/villin family of actin regulatory proteins. J. Cell Sci. 111, 2129–2136.
| 1:CAS:528:DyaK1cXlsF2itb8%3D&md5=18247fa818e407b8b78531ccf000a7f2CAS | 9664034PubMed |

Memili, E., and First, N. L. (1998). Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of alpha-amanitin on embryo development. Mol. Reprod. Dev. 51, 381–389.
| Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of alpha-amanitin on embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnt1Ortrw%3D&md5=0b9679c23715b48da690e296fb9d3a82CAS | 9820196PubMed |

Memili, E., Dominko, T., and First, N. L. (1998). Onset of transcription in bovine oocytes and preimplantation embryos. Mol. Reprod. Dev. 51, 36–41.
| Onset of transcription in bovine oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltVGltbc%3D&md5=8bf759a0d9551a4a5769d5df46148b3aCAS | 9712315PubMed |

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 | 1:CAS:528:DC%2BC3sXjsFOhu74%3D&md5=72be54a3e89051b46cce7e47628821a6CAS | 23463315PubMed |

Mercer, T. R., Dinger, M. E., and Mattick, J. S. (2009). Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 10, 155–159.
| Long non-coding RNAs: insights into functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFGlu7k%3D&md5=0540c0c0e9a8e22c071770f53b55e1e8CAS | 19188922PubMed |

Minchiotti, G., Parisi, S., Liguori, G. L., D’Andrea, D., and Persico, M. G. (2002). Role of the EGF-CFC gene cripto in cell differentiation and embryo development. Gene 287, 33–37.
| Role of the EGF-CFC gene cripto in cell differentiation and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFygt7k%3D&md5=58bdca743547807445b02094c0e1c83bCAS | 11992720PubMed |

Morris, K. V. (2012). ‘Non-coding RNAs and Epigenetic Regulation of Gene Expression: Drivers of Natural Selection.’ (Caister Academic Press: La Jolla, CA, USA.)

Nagaso, H., Murata, T., Day, N., and Yokoyama, K. K. (2001). Simultaneous detection of RNA and protein by in situ hybridization and immunological staining. J. Histochem. Cytochem. 49, 1177–1182.
| Simultaneous detection of RNA and protein by in situ hybridization and immunological staining.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsFyltLg%3D&md5=1e419e8fd9eb869b7d8a74a5f1780da2CAS | 11511686PubMed |

Paradis, F., Vigneault, C., Robert, C., and Sirard, M. A. (2005). RNA interference as a tool to study gene function in bovine oocytes. Mol. Reprod. Dev. 70, 111–121.
| RNA interference as a tool to study gene function in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlSksw%3D%3D&md5=78b202c515c5ad0ee11fcb48f681bf96CAS | 15570624PubMed |

Pauli, A., Rinn, J. L., and Schier, A. F. (2011). Non-coding RNAs as regulators of embryogenesis. Nat. Rev. Genet. 12, 136–149.
| Non-coding RNAs as regulators of embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVeltg%3D%3D&md5=239864291bfa5db445f7d2e9f903e46eCAS | 21245830PubMed |

Perkel, J. M. (2013). Visiting ‘noncodarnia’. Biotechniques 54, 301, 303–304.
| Visiting ‘noncodarnia’.Crossref | GoogleScholarGoogle Scholar |

Petrovic, V., and Piquette-Miller, M. (2010). Impact of polyinosinic/polycytidylic acid on placental and hepatobiliary drug transporters in pregnant rats. Drug Metab. Dispos. 38, 1760–1766.
| Impact of polyinosinic/polycytidylic acid on placental and hepatobiliary drug transporters in pregnant rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1eisLnN&md5=598cd364ef3de64ac91a634a80d5123aCAS | 20610559PubMed |

Piqué, M., López, J. M., Foissac, S., Guigó, R., and Méndez, R. (2008). A combinatorial code for CPE-mediated translational control. Cell 132, 434–448.
| A combinatorial code for CPE-mediated translational control.Crossref | GoogleScholarGoogle Scholar | 18267074PubMed |

Plante, L., Plante, C., Shepherd, D. L., and King, W. A. (1994). Cleavage and 3H-uridine incorporation in bovine embryos of high in vitro developmental potential. Mol. Reprod. Dev. 39, 375–383.
| Cleavage and 3H-uridine incorporation in bovine embryos of high in vitro developmental potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisFWjtro%3D&md5=7da412ebd2d7da15a2d8bcfc0c3aa879CAS | 7893486PubMed |

Plourde, D., Vigneault, C., Laflamme, I., Blondin, P., and Robert, C. (2012a). Cellular and molecular characterization of the impact of laboratory setup on bovine in vitro embryo production. Theriogenology 77, 1767–1778e1.
| Cellular and molecular characterization of the impact of laboratory setup on bovine in vitro embryo production.Crossref | GoogleScholarGoogle Scholar | 22365704PubMed |

Plourde, D., Vigneault, C., Lemay, A., Breton, L., Gagne, D., Laflamme, I., Blondin, P., and Robert, C. (2012b). Contribution of oocyte source and culture conditions to phenotypic and transcriptomic variation in commercially produced bovine blastocysts. Theriogenology 78, 116–131e3.
| Contribution of oocyte source and culture conditions to phenotypic and transcriptomic variation in commercially produced bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 22494684PubMed |

Rapicavoli, N. A., Qu, K., Zhang, J., Mikhail, M., Laberge, R. M., and Chang, H. Y. (2013). A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. Elife 2, e00762.
| A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics.Crossref | GoogleScholarGoogle Scholar | 23898399PubMed |

Rederstorff, M., and Huttenhofer, A. (2011). cDNA library generation from ribonucleoprotein particles. Nat. Protoc. 6, 166–174.
| cDNA library generation from ribonucleoprotein particles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVynur0%3D&md5=83948cd868120ff76d89b6d3a9e78eb5CAS | 21293458PubMed |

Renaud, S. J., Kubota, K., Rumi, M. A., and Soares, M. J. (2014). The FOS transcription factor family differentially controls trophoblast migration and invasion. J. Biol. Chem. 289, 5025–5039.
| The FOS transcription factor family differentially controls trophoblast migration and invasion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivF2lurk%3D&md5=956a1fbb8223a68e4846d87ca66fae01CAS | 24379408PubMed |

Robert, C., Nieminen, J., Dufort, I., Gagne, D., Grant, J. R., Cagnone, G., Plourde, D., Nivet, A. L., Fournier, E., Paquet, E., Blazejczyk, M., Rigault, P., Juge, N., and Sirard, M. A. (2011). Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays. Mol. Reprod. Dev. 78, 651–664.
| Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGns7vK&md5=e53ac4bb161cf485d1b52bc51d8ddbb1CAS | 21812063PubMed |

Scantland, S., Grenon, J. P., Desrochers, M. H., Sirard, M. A., Khandjian, E. W., and Robert, C. (2011). Method to isolate polyribosomal mRNA from scarce samples such as mammalian oocytes and early embryos. BMC Dev. Biol. 11, 8.
| Method to isolate polyribosomal mRNA from scarce samples such as mammalian oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXivVens7o%3D&md5=9508c4917dc06f6b060666123d14f7ffCAS | 21324132PubMed |

Schultz, R. M. (1993). Regulation of zygotic gene activation in the mouse. Bioessays 15, 531–538.
| Regulation of zygotic gene activation in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7otlWqsg%3D%3D&md5=d664b4eef5e20733444e727127343c48CAS | 8135766PubMed |

Sheik Mohamed, J., Gaughwin, P. M., Lim, B., Robson, P., and Lipovich, L. (2010). Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA 16, 324–337.
| Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 20026622PubMed |

Shojaei Saadi, H. A., O’Doherty, A. M., Gagne, D., Fournier, E., Grant, J. R., Sirard, M. A., and Robert, C. (2014). An integrated platform for bovine DNA methylome analysis suitable for small samples. BMC Genomics 15, 451.
| An integrated platform for bovine DNA methylome analysis suitable for small samples.Crossref | GoogleScholarGoogle Scholar | 24912542PubMed |

Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Gnirke, A., Regev, A., and Meissner, A. (2012). A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339–344.
| A unique regulatory phase of DNA methylation in the early mammalian embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xks1yrsbw%3D&md5=de248ce4dfeac66796f9c788a937d7f7CAS | 22456710PubMed |

Thermann, R., and Hentze, M. W. (2007). Drosophila miR2 induces pseudo-polysomes and inhibits translation initiation. Nature 447, 875–878.
| Drosophila miR2 induces pseudo-polysomes and inhibits translation initiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXms1Wjt78%3D&md5=db96813fafe9b4333f6a33d48af1d256CAS | 17507927PubMed |

Tripathi, V., Shen, Z., Chakraborty, A., Giri, S., Freier, S. M., Wu, X., Zhang, Y., Gorospe, M., Prasanth, S. G., Lal, A., and Prasanth, K. V. (2013). Long noncoding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB. PLoS Genet. 9, e1003368.
| Long noncoding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvValtbk%3D&md5=7965f171ddd6d0d83a5c6d048ed443dfCAS | 23555285PubMed |

Ulitsky, I., and Bartel, D. P. (2013). lincRNAs: genomics, evolution, and mechanisms. Cell 154, 26–46.
| lincRNAs: genomics, evolution, and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVGktrbP&md5=c4d1a42abd67d998483c781ba6826903CAS | 23827673PubMed |

Vallot, C., Huret, C., Lesecque, Y., Resch, A., Oudrhiri, N., Bennaceur-Griscelli, A., Duret, L., and Rougeulle, C. (2013). XACT, a long noncoding transcript coating the active X chromosome in human pluripotent cells. Nat. Genet. 45, 239–241.
| XACT, a long noncoding transcript coating the active X chromosome in human pluripotent cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSjtLw%3D&md5=bfcbff724c38f07b3ae0ecf35cba154eCAS | 23334669PubMed |

van Heesch, S., van Iterson, M., Jacobi, J., Boymans, S., Essers, P. B., de Bruijn, E., Hao, W., Macinnes, A. W., Cuppen, E., and Simonis, M. (2014). Extensive localization of long noncoding RNAs to the cytosol and mono- and polyribosomal complexes. Genome Biol. 15, R6.
| Extensive localization of long noncoding RNAs to the cytosol and mono- and polyribosomal complexes.Crossref | GoogleScholarGoogle Scholar | 24393600PubMed |

Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034–research0034.11.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar | 12184808PubMed |

Wang, K. C., Yang, Y. W., Liu, B., Sanyal, A., Corces-Zimmerman, R., Chen, Y., Lajoie, B. R., Protacio, A., Flynn, R. A., Gupta, R. A., Wysocka, J., Lei, M., Dekker, J., Helms, J. A., and Chang, H. Y. (2011). A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120–124.
| A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsVKrsro%3D&md5=96c3e49bad7c036b33868c5538c7c0f2CAS | 21423168PubMed |

Wilusz, J. E., Sunwoo, H., and Spector, D. L. (2009). Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 23, 1494–1504.
| Long noncoding RNAs: functional surprises from the RNA world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXos1GitLw%3D&md5=c8f7cce1be392295c813f13e0f0f91ecCAS | 19571179PubMed |

Wutz, A., and Gribnau, J. (2007). X inactivation Xplained. Curr. Opin. Genet. Dev. 17, 387–393.
| X inactivation Xplained.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Kku7zP&md5=85f5bec7aeba32409a705a1488264266CAS | 17869504PubMed |

Yan, L., Yang, M., Guo, H., Yang, L., Wu, J., Li, R., Liu, P., Lian, Y., Zheng, X., Yan, J., Huang, J., Li, M., Wu, X., Wen, L., Lao, K., Qiao, J., and Tang, F. (2013). Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1131–1139.
| Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1CgsLnO&md5=b7b70de6477cb52d6511d9e4e93d55adCAS | 23934149PubMed |