Contributions of RNA-seq to improve <i>in vitro</i> embryo production (IVP)

Santana, Priscila Di Paula Bessa; Silva, Artur Luis da Costa da; Ramos, Rommel Thiago Jucá; Gonçalves, Arnaldo Algaranhar; Costa, Nathalia Nogueira da; Ramos, Priscilla do Carmo Azevedo; Silva, Thiago Velasco Guimarães; Cordeiro, Marcela da Silva; Santos, Simone do Socorro Damasceno; Ohashi, Otávio Mitio; Miranda, Moysés dos Santos

doi:10.21451/1984-3143-AR2017-0043

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Reviews • Anim. Reprod. 16 (2) • Apr-Jun 2019 • https://doi.org/10.21451/1984-3143-AR2017-0043 copy

Contributions of RNA-seq to improve in vitro embryo production (IVP)

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

In Vitro Embryo Production (IVP) is widely used to improve the reproductive efficiency of livestock animals, however increasing the embryo development rates and pregnancy outcomes is still a challenge for some species. Thus, the lack of biological knowledge hinders developing specie-specific IVP protocols. Therefore, the contributions of RNA-seq to generate relevant biological knowledge and improve the efficiency of IVP in livestock animals are reviewed herein.

Keywords:
biomarker genes; in vitro embryo production; livestock animals; RNA-seq

Applications of RNA-seq	Reference	Specie	RNA-seq plataform	Brief summary of experimental design
Produce dataset of EST to design probes and a new microarray platform	*Robert et al. (2011)*Robert C, Nieminen J, Dufort I, Gagné D, Grant JR, Cagnone G, Plourde D, Nivet A, Fournier É, Paquet É, Blazejczyk M, Rigault P, Juge N, Sirard M. 2011. Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays. Mol Reprod Dev, 78:651-664.	Bovine	Genome Sequencer FLX, 454 Life Sciences	Sequencing of germinal vesicle oocyte, 2-, 4-, 8-, 16-cells, morula, blastocyst and hatched blastocyst produced in vitro and derived in vivo
	*Tsoi et al. (2012)*Tsoi S, Zhou C, Grant JR, Pasternak JA, Dobrinsky J, Rigault P, Nieminen J, Sirard MA, Robert C, Foxcroft GR, Dyck MK. 2012. Development of a porcine (Sus scofa) embryo-specific microarray: array annotation and validation. BMC Genomics, 3(13):370. Doi: 10.1186/1471-2164-13-370. https://doi.org/10.1186/1471-2164-13-370...	Porcine	Genome Sequencer FLX, 454 Life Sciences	Sequencing of germinal vesicle, metaphase II oocyte, 2-, 4-, 8-, morula, expanded and hatched blastocyst produced in vitro and derived in vivo
Study oocyte competence	*Macaulay et al. (2014)*Macaulay AD, Gilbert I, Caballero J, Barreto R, Fournier E, Tossou P, Sirard MA, Clarke HJ, Khandjian ÉW, Richard FJ, Hyttel P, Robert C. 2014. The gametic synapse: RNA transfer to the bovine oocyte. Biol Reprod, 91(4):90. Doi: 10.1095/biolreprod.114.119867. https://doi.org/10.1095/biolreprod.114.1...	Bovine	Illumina, HiSeq 2000	Comparison of germinal vesicle versus metaphase II oocytes matured in vitro
	*Reyes et al. (2015)*Reyes JM, Chitwood JL, Ross PJ. 2015. RNA-Seq profiling of single bovine oocyte transcript abundance and its modulation by cytoplasmic polyadenylation. Mol Reprod Dev, 82(2):103-114.	Bovine	Illumina, HiSeq 2000	Comparison of polyadenylated transcripts in germinal vesicle versus metaphase II oocytes matured in vitro
	*Macaulay et al. (2016)*Macaulay AD, Gilbert I, Scantland S, Fournier E, Ashkar F, Bastien A, Saadi HA, Gagné D, Sirard MA, Khandjian ÉW, Richard FJ, Hyttel P, Robert C. 2016. Cumulus Cell Transcripts Transit to the Bovine Oocyte in Preparation for Maturation. Biol Reprod, 94(1):16. Doi: 10.1095/biolreprod.114.127571. https://doi.org/10.1095/biolreprod.114.1...	Bovine	Illumina, HiSeq 2000	Comparison of germinal vesicle versus metaphase II oocytes in vitro matured versus total RNA found in the TZPs
	*Gilchrist et al. (2016)*Gilchrist GC, Tscherner A, Nalpathamkalam T, Merico D, LaMarre J. 2016. MicroRNA Expression during Bovine Oocyte Maturation and Fertilization. Int J Mol Sci, 17(3):396. Doi: 10.3390/ijms17030396. https://doi.org/10.3390/ijms17030396...	Bovine	Illumina, HiSeq 2500	Comparison of germinal vesicle versus metaphase II oocytes versus presumptive zygotes
Study non-invasive mRNA and miRNA biomarkers of oocyte competence	*Luo et al. (2016)*Luo F, Jia R, Ying S, Wang Z, Wang F. 2016. Analysis of genes that influence sheep follicular development by different nutrition levels during the luteal phase using expression profiling. Anim Genet, 47(3):354-364.	Sheep	Illumina, HiSeq 2000	Comparison of granulosa cells isolated from animals short-term dietary-restricted versus nutrient-supplemented
	*Wu et al. (2017)*Wu Y, Lin J, Li X, Han B, Wang L, Liu M, Huang J. 2017. Transcriptome profile of one-month-old lambs’ granulosa cells after superstimulation. Asian-Australas J Anim Sci, 30(1):20-33.	Sheep	Illumina, HiSeq 2500	Comparison of granulosa cells isolated from prepubertal versus adult superstimulated follicles
	*Mazzoni et al. (2017)*Mazzoni G, Salleh SM, Freude K, Pedersen HS, Stroebech L, Callesen H, Hyttel P, Kadarmideen HN. 2017. Identification of potential biomarkers in donor cows for in vitro embryo production by granulosa cell transcriptomics. PLoS ONE, 12(4):e0175464.	Bovine	Illumina, HiSeq 2500	Sequencing of granulosa cells collected at OPU prior to IVEP. Follow IVEP and correlation of the blastocyst rates with RNA-seq results
Study transcriptomic profile and molecular markers of sperm quality	*Card et al. (2013)*Card CJ, Anderson EJ, Zamberlan S, Krieger KE, Kaproth M, Sartini BL. 2013. Cryopreserved bovine spermatozoal transcript profile as revealed by high-throughput ribonucleic acid sequencing. Biology of Reproduction, 88(2):1-9.	Bovine	Illumina, HiSeq 2000	Sequencing of cryopreserved spermatozoa
	*Kropp et al. (2017)*Kropp J, Carrillo JA, Namous H, Daniels A, Salih SM, Song J, Khatib H. 2017. Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genomics, 18(1):280. Doi: 10.1186/s12864-017-3673-y. https://doi.org/10.1186/s12864-017-3673-...	Bovine	Illumina, HiSeq 2000	Comparison of blastocysts derived from low-fertility versus high-fertility bull (based on SCR)
	*Selvaraju et al. (2017)*Selvaraju S, Parthipan S, Somashekar L, Kolte AP, Krishnan Binsila B, Arangasamy A, Ravindra JP. 2017. Occurrence and functional significance of the transcriptome in bovine (Bos taurus) spermatozoa. Sci Rep, 7:42392.	Bovine	Ion ProtonTM and Illumina, HiSeq 2000	Use of two NGS platafforms to sequence spermatozoa cells obtained from fresh semen
	*Gòdia et al. (2018)*Gòdia M, Mayer FQ, Nafissi J, Castelló A, Rodríguez-Gil JE, Sánchez A, Clop A. 2018. A technical assessment of the porcine ejaculated spermatozoa for a sperm-specific RNA-seq analysis. Syst Biol Reprod Med, 26:1-13.	Porcine	Illumina, HiSeq 2000	Optimization of methodological workflow for RNA-seq of spermatozoa from fresh semen
Study the onset of EGA	Ostrup et al. (2013)	Porcine	SOLiD, Applied Biosystems	Comparison of 2- and 4-cells embryos in vitro produced versus in vivo derived
	*Graf et al. (2014)*Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E. 2014. Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc Natl Acad Sci U S A, 111(11):4139-4144.	Bovine	Illumina, GAIIx	Comparison of germinal vesicle oocyte, metaphase II oocyte, 4-, 8-, 16-cells and blastocysts produced in vitro
	*Jiang et al. (2014)*Jiang Z, Sun J, Dong H, Luo O, Zheng X, Obergfell C, Tang Y, Bi J, O'Neill R, Ruan Y, Chen J, Tian X. 2014. Transcriptional profiles of bovine in vivo pre-implantation development. BMC Genomics, 15(1):756. Doi: 10.1186/1471-2164-15-756. https://doi.org/10.1186/1471-2164-15-756...	Bovine	SOLiD, Applied Biosystems	Comparison of metaphase II oocyte, 2-, 4-, 8-, 16-cells, early morula, late morula and blastocyst derived in vivo
	*Jiang et al. (2015)*Jiang Z, Dong H, Zheng X, Marjani SL, Donovan DM, Chen J, Tian XC. 2015. mRNA Levels of Imprinted Genes in Bovine In Vivo Oocytes, Embryos and Cross Species Comparisons with Humans, Mice and Pigs. Sci Rep, 5:17898. Doi:10.1038/srep17898. https://doi.org/10.1038/srep17898...	Bovine, human, mice and pig	RNA-seq data downloaded from online database	Comparison of metaphase II oocyte, 2-, 4-, 8-, 16-cells, early morula, late morula and blastocyst derived in vivo
Study the IVF effects on embryo development	*Bauer et al. (2010)*Bauer BK, Isom SC, Spate LD, Whitworth KM, Spollen WG, Blake SM, Springer GK, Murphy CN, Prather RS. 2010. Transcriptional Profiling by Deep Sequencing Identifies Differences in mRNA Transcript Abundance in In Vivo-Derived Versus In Vitro-Cultured Porcine Blastocyst Stage Embryos. Biol Reprod, 83(5):791-798.	Porcine	Illumina, GAIIx	Comparison of blastocysts in vivo derived versus collected from uterus at 2-4-cells further in vitro cultured until blastocyst stage
	Huang and Khatib (2010)Huang W, Khatib H. 2010. Comparison of transcriptomic landscapes of bovine embryos using RNA-Seq. BMC Genomics, 11(1):711. Doi: 10.1186/1471-2164-11-711. https://doi.org/10.1186/1471-2164-11-711...	Bovine	Illumina, GAIIx	Comparison of fully developed in vitro blastocyst versus arrested embryos (failed to develop from morula to blastocyst stage)
	*Redel et al. (2012)*Redel BK, Brown AN, Spate LD, Whitworth KM, Green JA, Prather RS. 2012. Glycolysis in preimplantation development is partially controlled by the Warburg Effect. Mol Reprod Dev, 79(4):262-271.	Porcine	Illumina, GAIIx	Comparison of embryos in vitro cultured in low or high O2 atmospheres
	*Driver et al. (2012)*Driver AM, Penagaricano F, Huang W, Ahmad KR, Hackbart KS, Witlbank MC, Khatib H. 2012. RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo- and in vitro-derived bovine blastocysts. BMC Genomics, 13(1):118.	Bovine	Illumina, Hiseq 2000	Comparison of in vitro and in vivo blastocysts with similar quality grade
	*Cao et al. (2014)*Cao S, Han J, Wu J, Li Q, Liu S, Zhang W, Pei Y, Ruan X, Liu Z, Wang X, Lim B, Ning L. 2014. Specific gene-regulation networks during the pre-implantation development of the pig embryo as revealed by deep sequencing. BMC Genomics, 15:4. Doi.org/10.1186/1471-2164-15-4. https://doi.org/Doi.org/10.1186/1471-216...	Porcine	SOLiD 4, Applied Biosystems	Comparison of 1-, 2-, 4-, 8-cells, morula and blastocysts in vivo derived versus produced in vitro using SCNT biotechnology
	*Hera et al.* (2016)**Heras S, De Coninck DIM, Van Poucke M, Goossens K, Bogado Pascottini O, Van Nieuwerburgh F, Deforce D, De Sutter P, Leroy JLMR, Gutierrez-Adan A, Peelman L, Van Soom A. 2016. Suboptimal culture conditions induce more deviations in gene expression in male than female bovine blastocysts. BMC Genomics, 17:72. Doi: 10.1186/s12864-016-2393-z. https://doi.org/10.1186/s12864-016-2393-...	Bovine	Illumina, HiSeq 2500	Comparison of blastocysts in vitro produced in serum-containing media versus serum free-media versus blastocysts derived in vivo
	*Milazzoto et al.* (2016)**Milazzotto MP, Goissis MD, Chitwood JL, Annes K, Soares CA, Ispada J, Assumpção ME, Ross PJ. 2016. Early cleavages influence the molecular and the metabolic pattern of individually cultured bovine blastocysts. Mol Reprod Dev, 83(4):324-336.	Bovine	Illumina, HiSeq 2000	Comparison of slow and fast-cleavage embryos in vitro produced versus embryos derived in vivo
Study non-invasive mRNA and miRNA biomarkers of embryo quality	*Kropp et al. (2014)*Kropp J, Salih SM, Khatib H. 2014. Expression of microRNAs in bovine and human pre-implantation embryo culture media. Front Genet, 5:91. Doi: 10.3389/fgene.2014.00091. https://doi.org/10.3389/fgene.2014.00091...	Bovine	Illumina, GAIIx	Comparison of media conditioned by fully developed blastocysts versus arrested embryos (failed to develop from morula to blastocyst)
	Kropp and Khatib (2015)Kropp J, Khatib H. 2015. mRNA fragments in in vitro culture media are associated with bovine preimplantation embryonic development. Front Genet, 6:273. Doi: 10.3389/fgene.2015.00273. https://doi.org/10.3389/fgene.2015.00273...	Bovine	Illumina, GAIIx	Comparison of media conditioned by fully developed blastocysts versus arrested embryos (failed to develop from morula to blastocyst)

Source	Putative biomarker genes
MII oocyte	CCNB1, WEE2, FBXO43, MELK, H1FOO, RALB, ZP2, IGF2R, miRNA-155, miRNA-222, miRNA-21 and miRNA-190a
Transzonal projections	ZNF773, ZNF689, ZNF75A, ZNF664, ZNF395, FAM21 and WASF2
Cumulus cells	GATM, Mx1 and STC1
Spermatozoa	CLU, AKAP4, PRM1, PRM2, PLCZ1, CRISP2, PSG-1, HLA-E, DBY, EIF1, EIF5, EEF1A1, EEF1γ, TFB2M and CYCS
Blastocyst	DNMT3A, GATA3, CD9, ATP6V0A4, FAM115C, LGALS1, SLC9A3R1, BCAM, BPIFA1, PLXNA3, SHROOM2, SLC16A7, EEF2, RPL10A and RPL38
IVC-conditioned media	POSTN, VSNL-1, PUM2, miRNA-181a2, miRNA-196a2, miRNA-302c, and miRNA-25

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[1] §Corresponding author: ppbsantana@gmail.com