Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2017-0043
Animal Reproduction (AR)
Review

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

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

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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.

References

Abe H, Yamashita S, Satoh T, Hoshi H. 2002. Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Mol Reprod Dev, 61(1):57-66.

Ahn HW, Farmer JL, Bazer FW, Spencer TE. 2009. Progesterone and interferon tau regulated genes in the ovine uterine endometrium: identification of periostin as a potential mediator of conceptus elongation. Reproduction, 1(138):813-825.

Ambros V. 2001. microRNAs: tiny regulators with great potential. Cell, 28(107):823-836.

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.

Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. 2010. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod, 16(3):135-152.

Betts DH, Bain NT, Madan P. 2014. The p66(Shc) adaptor protein controls oxidative stress response in early bovine embryos. PloS One, 9(1):e86978.

Brosens JJ, Salker MS, Teklenburg G, Nautiyal J, Salter S, Lucas ES, Steel JH, Christian M, Chan YW, Boomsma CM, Moore JD, Hartshorne GM, Sućurović S, Mulac-Jericevic B, Heijnen CJ, Quenby S, Koerkamp MJ, Holstege FC, Shmygol A, Macklon NS. 2014. Uterine selection of human embryos at implantation. Sci Rep, 4:3894. Doi: 10.1038/srep03894.

Bunel A, Jorssen EP, Merckx E, Leroy JL, Bols PE, Sirard MA. 2015. Individual bovine in vitro embryo production and cumulus cell transcriptomic analysis to distinguish cumulus-oocyte complexes with high or low developmental potential. Theriogenology, 83(2):228-237.

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.

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.

Comizzoli P, Songsasen N, Wildt DE. 2010. Protecting and extending fertility for females of wild and endangered mammals. Cancer Treat Res, 156:87-100.

Corcoran D, Fair T, Park S, Rizos D, Patel OV, Smith GW, Coussens PM, Ireland JJ, Boland MP, Evans ACO, Lonergan P. 2006. Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos. Reproduction, 131(4):651-660.

Costa NN, Cordeiro MS, Silva TV, Sastre D, Santana PP, Sá AL, Sampaio RV, Santos SS, Adona PR, Miranda MS, Ohashi OM. 2013. Effect of triiodothyronine on developmental competence of bovine oocytes. Theriogenology, 80(4):295-301.

De Souza-Fabjan JMG, Panneau B, Duffard N, Locatelli Y, De Figueiredo JR, Freitas VJF, Mermillod P. 2014. In vitro production of small ruminant embryos: late improvements and further research. Theriogenology, 81(9):1149-1162.

Di Francesco S, Boccia L, Campanile G, Di Palo R, Vecchio D, Neglia G, Zicarelli L, Gasparrini B. 2011. The effect of season on oocyte quality and developmental competence in Italian Mediterranean buffaloes (Bubalus bubalis). Anim Reprod Sci, 123(1-2):48-53.

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.

Dyck MK, Zhou C, Tsoi S, Grant J, Dixon WT, Foxcroft GR. 2014. Reproductive technologies and the porcine embryonic transcriptome. Anim Reprod Sci, 149(1), 11-18.

Feuerstein P, Puard V, Chevalier C, Teusan R, Cadoret V, Guerif F, Houlgatte R, Royere D. 2012. Genomic assessment of human cumulus cell marker genes as predictors of oocyte developmental competence: impact of various experimental factors. PloS One, 7(7):e40449.

Gasparrini B, Neglia G, Di Palo R, Vecchio D, Albero G, Esposito L, Campanile G, Zicarelli L. 2014. Influence of oocyte donor on in vitro embryo production in buffalo. Anim Reprod Sci, 144(3-4):95-101.

George F, Daniaux C, Genicot G, Verhaeghe B, Lambert P, Donnay I. 2008. Set up of a serum-free culture system for bovine embryos: embryo development and quality before and after transient transfer. Theriogenology, 69(5):612-623.

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.

Gilchrist RB, Thompson JG. 2007. Oocyte maturation: Emerging concepts and technologies to improve developmental potential in vitro. Theriogenology, 67(1):6-15.

Gilchrist RB, Lane M, Thompson JG. 2008. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update, 14(2):159-177.

Glenn TC. 2011. Field guide to next-generation DNA sequencers. Mol Ecol Resour, 11(5):759-769.

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.

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.

Grupen CG. 2014. The evolution of porcine embryo in vitro production. Theriogenology, 81(1):24-37.

Han Y, Gao S, Muegge K, Zhang W, Zhou B. 2015. Advanced Applications of RNA Sequencing and Challenges. Bioinform Biol Insights, 9(Suppl 1):29-46.

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.

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.

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.

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.

Kasinathan P, Wei H, Xiang T, Molina JA, Metzger J, Broek D, Kasinathan S, Faber DC, Allan MF. 2015. Acceleration of genetic gain in cattle by reduction of generation interval. Sci Rep, 5:8674. Doi:10.1038/srep08674.

Kątska-Książkiewicz L, Opiela J, Ryńska B. 2007. Effects of oocyte quality, semen donor and embryo co-culture system on the efficiency of blastocyst production in goats. Theriogenology, 68(5):736-744.

Knobil E, Neill JD, Hess AP, Nayak NR, Giudice LC. 2006. Knobil And Neill’s Physiology of Reproduction (3nd ed). In: J.D. Neill (Ed.). St. Louis, USA: Elsevier Academic Press, p.337.

Krawetz, AS. 2005. Paternal contribution: new insights and future challenges. Nat Rev Genet, 6:633-642.

Krisher RL, Lane M, Bavister BD. 1999. Developmental Competence and Metabolism of Bovine Embryos Cultured in Semi-Defined and Defined Culture Media. Biol Reprod, 60(6):1345-1352.

Krisher RL, Prather RS. 2012. A role for the Warburg Effect in preimplantation embryo development: Metabolic modification to support rapid cell proliferation. Mol Reprod Dev, 79(5):311-20. Doi: 10.1002/mrd.22037.

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.

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.

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.

Kumar P, Verma A, Roy B, Rajput S, Ojha S, Anand S, Yadav P, Arora J, De S, Goswami SI, Datta TK. 2012. Effect of Varying Glucose Concentrations during In Vitro Maturation and Embryo Culture on Efficiency of In Vitro Embryo Production in Buffalo. Reprod Domest Anim, 47(2):269-273.

Labrecque R, Sirard MA. 2014. The study of mammalian oocyte competence by transcriptome analysis: progress and challenges. Mol Hum Reprod, 20(2):103-116.

Lima JS, Leão DL, Sampaio RV, Brito AB, Santos RR, Miranda MS, Ohashi OM, Domingues SFS. 2013. Embryo production by parthenogenetic activation and fertilization of in vitro matured oocytes from Cebus apella. Zygote, 21(2):162-166.

Liu L, Li Y, Li S, Hu N, He Y, Pong R, Lin D, Lu L, Law M. 2012. Comparison of next-generation sequencing systems. J Biomed Biotechnol, 2012:251364. Doi:10.1155/2012/251364.

Lonergan P, Fair T, Corcoran D, Evans AC. 2006. Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology, 65(1):137-152.

Lonergan P, Rizos D, Gutierrez-Adan A, Fair T, Boland MP. 2003. Effect of culture environment on embryo quality and gene expression - experience from animal studies. Reprod Biomed Online, 7(6):657-663.

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.

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.

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.

Macklon NS, Brosens JJ. 2014. The human endometrium as a sensor of embryo quality. Biol Reprod, 91(4):98. Doi: 10.1095/biolreprod.114.122846.

Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, Heyman Y, Galio L, Hue I, Yang X, Tian XC, Lewin HA, Renard JP. 2009. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci U S A, 106(14):5687-5692.

Mara L, Sanna D, Casu S, Dattena M, Mayorga Muñoz IM. 2013. Blastocyst rate of in vitro embryo production in sheep is affected by season. Zygote, 22:366-371.

Martin JA, Wang Z. 2011. Next-generation transcriptome assembly. Nat Rev Genet, 12(10):671-682.

Masudul Hoque SA, Yahia Khandoker MAM, Kabiraj SK, Asad LY, Fakruzzaman M, Tareq KMA. 2012. Effect of Goat Follicular Fluid on in vitro Production of Embryos in Black Bengal Goats. Iranian Journal of Applied Animal Science, 2(3): 287-294.

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.

Memili E, First NL. 1998. Developmental changes in RNA polymerase II in bovine oocytes, early embryos, and effect of alpha-amanitin on embryo development. Mol Reprod Dev, 51(4):381-389.

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.

Naderi MM, Borjian Boroujeni S, Sarvari A, Heidari B, Akhondi MM, Zarnani AH, Shirazi A. 2016. The Effect of Media Supplementation with Angiotensin on Developmental Competence of Ovine Embryos Derived from Vitrified-warmed Oocytes. Avicenna J Med Biotechnol, 8(3):139-144.

Nguyen BX, Kikuchi K, Uoc NT, Dang-Nguyen TQ, Linh NV, Men NT, Nguyen TT, Nagai T. 2015. Production of Ban miniature pig embryos by in vitro fertilization: A comparative study with Landrace. Anim Sci J, 86(5):487-493.

Niemann H, Wrenzycki C. 2000. Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology, 53(1):21-34.

Østrup O, Olbricht G, Østrup E, Hyttel P, Collas P, Cabot R. 2013. RNA profiles of porcine embryos during genome activation reveal complex metabolic switch sensitive to in vitro conditions. PloS One, 8(4):e61547.

Paramio MT, Izquierdo D. 2014. Current Status of In Vitro Embryo Production in Sheep and Goats. Reprod Domest Anim, 49(Suppl 4):37-48.

Pariset L, Chillemi G, Bongiorni S, Romano Spica V, Valentini A. 2009. Microarrays and high-throughput transcriptomic analysis in species with incomplete availability of genomic sequences. N Biotechnol, 25(5):272-279.

Parrish JJ. 2014. Bovine in vitro fertilization: in vitro oocyte maturation and sperm capacitation with heparin. Theriogenology, 81(1):67-73.

Prather R, Redel B, Whitworth K, Zhao M. 2014. Genomic profiling to improve embryogenesis in the pig. - PubMed - NCBI. Anim Reprod Sci, 149(1–2):39-45.

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.

Redel BK, Tessanne KJ, Spate LD, Murphy CN, Prather RS. 2015. Arginine increases development of in vitro-produced porcine embryos and affects the protein arginine methyltransferase–dimethylarginine dimethylaminohydrolase–nitric oxide axis. Reprod Fertil Dev, 27(4):655-666.

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.

Rizos D, Clemente M, Bermejo-Alvarez P, De La Fuente J, Lonergan P, Gutiérrez-Adán A. 2008. Consequences of in vitro culture conditions on embryo development and quality. Reprod Dom Anim, 43(Suppl 4):44-50.

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.

Rodríguez-Dorta N, Cognié Y, González F, Poulin N, Guignot F, Touzé JL, Baril G, Cabrera F, Alamo D, Batista M, Gracia A, Mermillod P. 2007. Effect of coculture with oviduct epithelial cells on viability after transfer of vitrified in vitro produced goat embryos. Theriogenology, 68(6):908-913.

Ruan YC, Guo JH, Liu X, Zhang R, Tsang LL, Dong JDA, Chen H, Yu MK, Jiang X, Zhang XH, Fok KL, Chung YW, Huang H, Zhou WL, Chan HC. 2012. Activation of the epithelial Na+ channel triggers prostaglandin E₂ release and production required for embryo implantation. Nat Med, 18(7):1112-1117.

Salvemini M, Arunkumar KP, Nagaraju J, Sanges R, Petrella V, Tomar A, Zhang H, Zheng W, Saccone G. (2014). De Novo Assembly and Transcriptome Analysis of the Mediterranean Fruit Fly Ceratitis capitata Early Embryos. PLoS ONE, 9(12):e114191. Doi: 10.1371/journal.pone.0114191. eCollection 2014.

Santana PPB, Silva TVG, Costa NN, Da Silva BB, Carter TF, Cordeiro MDS, Da Silva BJ, Santos SSD, Herculano AM, Adona PR, Ohashi OM, Miranda MD. 2014a. Supplementation of bovine embryo culture medium with L - arginine improves embryo quality via nitric oxide production. Mol Reprod Dev, 81(10):918-27. Doi: 10.1002/mrd.22387. Epub 2014 Sep 18.

Santana PPB, Carvalho CMF, Costa NN, Silva TVG, Ramos PCA, Cordeiro MS, Santos SS, Khayat AS, Ohashi OM, Miranda MS. 2014b. Effect of dexamethasone on development of in vitro-produced bovine embryos. Theriogenology, 82(1):10-16.

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.

Shirazi A, Ardali MA, Ahmadi E, Nazari H, Mamuee M, Heidari B. 2012. The Effect of Macromolecule Source and Type of Media During in vitro Maturation of Sheep Oocytes on Subsequent Embryo Development. J Reprod Infertil, 13(1):13-19.

Spate LD, Brown A, Redel BK, Whitworth KM, Prather RS. 2015. PS48 can replace bovine serum albumin in pig embryo culture medium, and improve in vitro embryo development by phosphorylating AKT. Mol Reprod Dev, 82(4):315-320.

Stringfellow DA, Seidel SM. (Eds). 1998. IETS. Manual of the international embryo transfer society. Savoy, Illinois, USA: International Embryo Transfer Society.

Tadros W, Lipshitz HD. 2009. The maternal-to-zygotic transition: a play in two acts. Development, 136(18):3033-3042.

Telford NA, Watson AJ, Schultz GA. 1990. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev, 26(1):90-100.

Tervit HR, Whittingham DG, Rowson LE. 1972. Successful culture in vitro of sheep and cattle ova. J Reprod Fertil, 30(3):493-497.

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.

Van Soom A, Mateusen B, Leroy J, De Kruif A. 2003. Assessment of mammalian embryo quality: what can we learn from embryo morphology? Reprod Biomed Online, 7(6):664-670.

Vander Heiden MG, Cantley LC, Thompson CB. 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science, 324(5930):1029-1033.

VanGuilder HD, Vrana KE, Freeman WM. 2008. Twenty-five years of quantitative PCR for gene expression analysis. BioTechniques, 44(5):619-626.

Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews. Genetics, 10(1):57-63.

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.

Yoshioka K, Noguchi M, Suzuki C. 2012. Production of piglets from in vitro-produced embryos following non-surgical transfer. Anim Reprod Sci, 131(1), 23-29.

Yuan Y, Spate LD, Redel BK, Tian Y, Zhou J, Prather RS, Roberts RM. 2017. Quadrupling efficiency in production of genetically modified pigs through improved oocyte maturation. Proc Natl Acad Sci U S A, 114(29):E5796-E5804.  doi: 10.1073/pnas.1703998114.

Zhao S, Fung-Leung WP, Bittner A, Ngo K, Liu X. 2014. Comparison of RNA-Seq and microarray in transcriptome profiling of activated T cells. PLoS One, 9(1):e78644. Doi: 10.1371/journal.pone.0078644.

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