Animal Reproduction (AR)
Animal Reproduction (AR)
Congress Paper

Embryo competence and cryosurvival: Molecular and cellular features

Thamiris V. Marsico, Janine de Camargo, Roniele S. Valente, Mateus J. Sudano

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Global cattle genetic market is experiencing a change of strategy, large genetic companies, traditionally recognized in the artificial insemination field, have also begun to operate in the embryo market. Consequently, the demand for in vitro produced (IVP) embryos has grown. However, the overall efficiency of the biotechnology process remains low. Additionally, the lack of homogeneity of post-cryopreservation survival results of IVP embryos still impairing a massive dissemination of this biotechnology in the field. A great challenge for in vitro production labs is to increase the amount of embryos produced with exceptional quality after each round of in vitro fertilization. Herein, we discuss the molecular and cellular features associated with the competence and cryosurvival of IVP embryos. First, morphofunctional, cellular and molecular competence of the embryos were addressed and a relationship between embryo developmental ability and quality were established with cryosurvival and pregnancy success. Additionally, determinant factors of embryo competence and cryosurvival were discussed including the following effects: genotype, oocyte quality and follicular microenvironment, in vitro production conditions, and lipids and other determining molecules. Finally, embryo cryopreservation aspects were addressed and an embryofocused approach to improve cryosurvival was presented.


in vitro production of embryos, bovine, embryo quality, cryopreservation, cryotolerance, pregnancy success.


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, 61:57-66.

Annes K, Müller DB, Vilela JAP, Valente RS, Caetano DP, Cibin FWS, Milazzotto MP, Mesquita FS, Belaz KRA, Eberlin MN, Sudano MJ. 2018. Influence of follicle size on bovine oocyte lipid composition, follicular metabolic and stress markers, embryo development and blastocyst lipid content. Reprod Fertil Dev, 31:462-472.

Arav A, Natan Y, Kalo D, Komsky-Elbaz A, Roth Z, Levi-Setti PE, Leong M, Patrizio P. 2018. A new, simple, automatic vitrification device: preliminary results with murine and bovine oocytes and embryos. J Assist Reprod Genet, 35:1161-1168.

Arreseigor CJ, Sisul A, Arreseigor AE, Stahringe RC. 1998. Effect of cryoprotectant, thawing method, embryo grade and breed on pregnancy rates of cryopreserved bovine embryos. Theriogenology, 49:160.

Báez F, Camargo A, Reyes AL, Márquez A, Paula-Lopes F, Viñolese C. 2019. Time-dependent effects of heat shock on the zona pellucida ultrastructure and in vitro developmental competence of bovine oocytes. Reprod Biol, 19:195-203.

BarcelóFimbres M, Seidel Jr G. 2007. Effects of fetal calf serum, phenazine ethosulfate and either glucose or fructose during in vitro culture of bovine embryos on embryonic development after cryopreservation. Mol Reprod Dev, 74:1395-1405.

Block J, Bonilla L, Hansen PJ. 2009. Effect of addition of hyaluronan to embryo culture medium on survival of bovine embryos in vitro following vitrification and establishment of pregnancy after transfer to recipients. Theriogenology, 71:1063-1071.

Bó G, Mapletoft RJ. 2013. Evaluation and classification of bovine embryos. Anim Reprod, 10:344-348.

Brackett BG, Zuelke KA. 1993. Analysis of factors involved in the in vitro production of bovine embryos. Theriogenology, 39:43-64.

Brevini Gandolfi TAL, Gandolfi F. 2001. The maternal legacy to the embryo: Cytoplasmic components and their effects on early development. Theriogenology, 55:1255-1276.

Castro S, de Andrade Carvalho A, Gomes da Silva CM, Rocha Faustino L, de Figueiredo JR, Ribeiro Rodrigues AP. 2011. Agentes crioprotetores intracelulares: características e utilização na criopreservação de tecido ovariano e oócitos. Acta Scientiae Veterinariae, 39:1-17.

Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell, 113:643-655.

Chiaratti MR, Ferreira CR, Perecin F, Meo SC, Sangalli JR, Mesquita LG, de Carvalho Balieiro JC, Smith LC, Garcia JM, Meirelles FV. 2011. Ooplast-mediated developmental rescue of bovine oocytes exposed to ethidium bromide. Reprod Biomed Online, 22:172-183.

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

Coskun S, Hellani A, Jaroudi K, Al-Mayman H, Al-Kabra M, Qeba M. 2003. Nucleolar precursor body distribution in pronuclei is correlated to chromosomal abnormalities in embryos. Reprod Biomed Online, 7:86-90.

Côté I, Vigneault C, Laflamme I, Laquerre J, Fournier É, Gilbert I, Scantland S, Gagné, D, Blondin P, 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.

D’Souza F, Uppangala S, Asampille G, Salian SR, Kalthur G, Talevi R, Atreya HS, Adiga SK. 2018. Spent embryo culture medium metabolites are related to the in vitro attachment ability of blastocysts. Sci Rep, 8:1-10.

Dalcin L, Lucci C. 2010. Criopreservação de embriões de animais de produção: princípios criobiológicos e estado atual. Rev Bras Reprod Anim, 34:149-159.

Dasiman R, Rahman NSA, Othman S, Mustafa MF, Mohd Yusoff NJ, Jusof WHW, Rajikin MH, Froemming GRA, Khan N. 2013. Cytoskeletal alterations in different developmental stages of in vivo cryopreserved preimplantation murine embryos. Med Sci Monit Basic Res, 19:258-266.

De Souza DK, Salles LP, Rosa E Silva A. 2015. Aspects of energetic substrate metabolism of in vitro and in vivo bovine embryos. Braz J Med Biol Res, 48:191-197.

Di Paolo G, De Camilli P. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature, 443:651-657

Dinnyés A, Carolan C, Lonergan P, Massip A, Mermillod P. 1996. Survival of frozen or vitrified bovine blastocysts produced in vitro in synthetic oviduct fluid. Theriogenology, 46:1425-1439.

Diskin MG, Sreenan JM. 1980. Fertilization and embryonic mortality rates in beef heifers after artificial insemination. J Reprod Fertil, 59:463-468.

El Shourbagy SH, Spikings EC, Freitas M, St John JC. 2006. Mitochondria directly influence fertilisation outcome in the pig. Reproduction, 131:233-245.

El-Sayed A, Hoelker M, Rings F, Salilew D, Jennen D, Tholen E, Sirard MA, Schellander K, 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.

Fahy GM, MacFarlane D, Angell C, Meryman H. 1984. Vitrification as an approach to cryopreservation. Cryobiology, 21:407-426.

Fair T, Lonergan P, Dinnyes A, Cottell DC, Hyttel P, Ward FA, Boland MP. 2001. Ultrastructure of bovine blastocysts following cryopreservation: effect of method of blastocyst production. Mol Reprod Dev, 58:186-195.

Fair T. 2003. Follicular oocyte growth and acquisition of developmental competence. Anim Reprod Sci, 78:203-216.

Fair T. 2010. Mammalian oocyte development: checkpoints for competence. Reprod Fertil Dev, 22:13-20.

Galli C, Lazzari G. 1996. Practical aspects of IVM/IVF in cattle. Anim Reprod Sci, 42:371-379.

Gardner DK, Leese HJ. 1988. The role of glucose and pyruvate transport in regulating nutrient utilization by preimplantation mouse embryos. Development, 104:423-429.

Ghanem N, Salilew-Wondim D, Gad A, Tesfaye D, Phatsara C, Tholen E, Looft C, Schellander K, Hoelker M. 2011. Bovine blastocysts with developmental competence to term share similar expression of developmentally important genes although derived from different culture environments. Reproduction, 142:551-564.

Gomez E, Munoz M, Rodriguez A, Caamano JN, Facal N, Diez C. 2009. Vitrification of bovine blastocysts produced in vitro inflicts selective damage to the inner cell mass. Reprod Domest Anim, 44:194-199.

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, 111:4139-4144.

Guillou H, Zadravec D, Martin PGP, Jacobsson A. 2010. The key roles of elongases and desaturases in mammalian fatty acid metabolism: Insights from transgenic mice. Prog Lipid Res, 49:186-199.

Hamatani T, Daikoku T, Wang H, Matsumoto H, Carter MG, Ko MS, Dey SK. 2004. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc Natl Acad Sci, 101:10326-31.

Hasler JF, Henderson WB, Hurtgen PJ, Jin ZQ, McCauley AD, Mower SA, Neely B, Shuey LS, Stokes JE, Trimmer SA. 1995. Production, freezing and transfer of bovine IVF embryos and subsequent calving results. Theriogenology, 43:141-152.

Hasler JF. 2000. In vitro culture of bovine embryos in Menezo’s B2 medium with or without coculture and serum: the normalcy of pregnancies and calves resulting from transferred embryos. Anim Reprod Sci, 60-61:81-91.

Held-Hoelker E, Klein S, Rings F, Salilew-Wondim D, Saeed-Zidane M, Neuhoff C, Tesfaye D, Schellander K, Hoelker M. 2017. Cryosurvival of in vitro produced bovine embryos supplemented with l-Carnitine and concurrent reduction of fatty acids. Theriogenology, 96:145-152.

Hoelker M, Held E, Salilew-Wondim D, Schellander K, Tesfaye D. 2014. Molecular signatures of bovine embryo developmental competence. Reprod Fertil Dev, 26:22-36.

Hoelker M, Schmoll F, Schneider H, Rings F, Gilles M, Tesfaye D, Jennen D, Tholen E, Griese J, Schellander K. 2006. Bovine blastocyst diameter as a

morphological tool to predict embryo cell counts, embryo sex, hatching ability and developmental characteristics after transfer to recipients. Reprod Fertil Dev, 18:551-557.

Holm P, Booth PJ, Callesen H. 2002. Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media. Reproduction, 123:553-565.

Hu K, Yu Y. 2017. Metabolite availability as a window to view the early embryo microenvironment in vivo. Mol Reprod Dev, 84:1027-1038.

Inaba Y, Aikawa Y, Hirai T, Hashiyada Y, Yamanouchi T, Misumi K, Ohtake M, Somfai T, Kobayashi S, Saito N, Matoba S, Konishi K, Imai K. 2011. In-straw cryoprotectant dilution for bovine embryos vitrified using Cryotop. J Reprod Dev, 57:437-443

Jiang Z, Sun J, Dong H, Luo O, Zheng X, Obergfell C, Tang Y, Bi J, O'Neill R, Ruan Y, Chen J, Tian XC. 2014. Transcriptional profiles of bovine in vivo pre-implantation development. BMC Genomics, 15:1-15.

Khurana NK, Niemann H. 2000. Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo. Biol Reprod, 62:847-856.

Kocyigit A, Cevik M. 2015. Effects of leukemia inhibitory factor and insulin-like growth factor-I on the cell allocation and cryotolerance of bovine blastocysts. Cryobiology, 71:64-69.

Kuwayama M. 2007. Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology, 67:73-80.

Labrecque R, Fournier E, Sirard MA. 2016. Transcriptome analysis of bovine oocytes from distinct follicle sizes: Insights from correlation network analysis. Mol Reprod Dev, 83:558-569.

Lane M, Schoolcraft WB, Gardner DK, Phil D. 1999. Vitrification of mouse and human blastocysts using a novel cryoloop container-less technique. Fertility and sterility, 72:1073-1078.

Latham KE. 2015. Endoplasmic reticulum stress signaling in mammalian oocytes and embryos: Life in the balance. Int Rev Cell Mol Biol, 316:227-265.

Lee HS, Ma H, Juanes RC, Tachibana M, Sparman M, Woodward J, Ramsey C, Xu J, Kang EJ, Amato P, Mair G, Steinborn R, Mitalipov S. 2012. Rapid mitochondrial DNA segregation in primate preimplantation embryos precedes somatic and germline bottleneck. Cell Rep, 1:506-515.

Leese HJ, Baumann CG, Brison DR, McEvoy TG, Sturmey RG. 2008. Metabolism of the viable mammalian embryo: Quietness revisited. Mol Hum Reprod, 14:667-672.

Leese HJ, Donnay I, Thompson JG. 1998. Human assisted conception: a cautionary tale. Lessons from domestic animals. Hum Reprod, 13:184-202.

Leese HJ, Sturmey RG, Baumann CG, McEvoy TG. 2007. Embryo viability and metabolism: Obeying the quiet rules. Hum Reprod, 22:3047-3050.

Leibo S. 1983. A one-step in situ dilution method for frozen thawed bovine embryos. Cryo-letters, 4:387-400.

Li S, Winuthayanon W. 2017. Oviduct: Roles in fertilization and early embryo development. J Endocrinol, 232:1-26.

Lin T, Lee JE, Kang JW, Oqani RK, Cho ES, Kim SB, Il Jin D. 2018. Melatonin supplementation during prolonged in vitro maturation improves the quality and development of poorquality porcine oocytes via antioxidative and antiapoptotic effects. Mol Reprod Dev, 85:665-681.

Lindner GM, Wright RW, Jr. 1983. Bovine embryo morphology and evaluation. Theriogenology, 20:407-416.

Liu L, Trimarchi JR, Keefe DL. 2000. Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes. Biol Reprod, 62:1745-1753.

Lledo B, Ortiz JA, Morales R, García-Hernández E, Ten J, Bernabeu A, Llácer J, Bernabeu R. 2018. Comprehensive mitochondrial DNA analysis and IVF outcome. Hum Reprod Open, 4:1-9.

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

Lonergan P, Fair T, Forde N, Rizos D. 2016. Embryo development in dairy cattle. Theriogenology, 86:270-277.

Lonergan P, Rizos D, Gutierrez-Adan A, Fair T, Boland MP. 2003. Oocyte and embryo quality: Effect of origin, culture conditions and gene expression patterns. Reprod Domest Anim, 38:259-267.

Lu KH, Gordon I, Gallagher M, Mcgovern H. 1987. Pregnancy established in cattle by transfer of embryos derived from invitro fertilization of oocytes matured in vitro. Vet Rec, 121:259-260.

Lundqvist M, Johansson U, Lundkvist O, Milton K, Westin C, Simberg N. 2001. Does pronuclear morphology and/or early cleavage rate predict embryo implantation potential? Reprod Biomed Online, 2:12-16.

Luo S, Mao C, Lee B, Lee AS. 2006. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol Cell Biol, 26:5688-5697.

Mahmoudzadeh AR, Van Soom A, Bols P, Ysebaert MT, de Kruif A. 1995. Optimization of a simple vitrification procedure for bovine embryos produced in vitro: effect of developmental stage, two-step addition of cryoprotectant and sucrose dilution on embryonic survival. J Reprod Fertil, 103:33-39.

Mao L, Lou H, Lou Y, Wang N, Jin F. 2014. Behaviour of cytoplasmic organelles and cytoskeleton during oocyte maturation. Reprod Biomed Online, 28:284-299.

Massip A. 1987. Recent progress in cryopreservation of cattle embryos. Theriogenology, 27:69-79.

Mattos MCC. Vitrificação e congelação de mórulas e blastocistos produzidos in vivo em bos taurus e bos indicus. [In portuguese]. Botucatu, Brazil: Universidade Estadual Paulista “Júlio de Mesquita Filho”. Dissertation.

May-Panloup P, Chretien MF, Jacques C, Vasseur C, Malthiery Y, Reynier P. 2005. Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum Reprod, 20:593-597.

Mazur P. 1980. Fundamental aspects of the freezing of cells, with emphasis on mammalian ova and embryos. In: International Congress on Animal Reproduction and Artificial Insemination. Proceedings of International Congress of Animal Reproduction and Artificial Insemination, pp.99-114.

McEvoy TG, Sinclair KD, Young LE, Wilmut I, Robinson JJ. 2000. Large offspring syndrome and other consequences of ruminant embryo culture in vitro: Relevance to blastocyst culture in human ART. Hum Fertil, 3:238-246.

Merton S, 2002. Morphological Evaluation of Embryos in Domestic Species. In: Van Soom A, Boerjan M. (Ed.) Assessment of Mammalian Embryo Quality. Springer Science+Business Media Dordrecht, pp429.

Miller DJ, Eckert JJ, Lazzari G, Duranthon-Richoux V, Sreenan J, Morris D, Galli C, Renard JP, Fleming TP. 2003. Tight junction messenger RNA expression levels in bovine embryos are dependent upon the ability to compact and in vitro culture methods. Biol Reprod, 68:1394-1402.

Misirlioglu M, Page GP, Sagirkaya H, Kaya A, Parrish JJ, First NL, Memili E. 2006. Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proc Natl Acad Sci U S A, 50:18905-18910.

Mogas T. 2019. Update on the vitrification of bovine oocytes and in vitro-produced embryos. Reprod Fertil Dev, 31:105-117.

Mondou E, Dufort I, Gohin M, Fournier E, Sirard MA. 2012. Analysis of microRNAs and their precursors in bovine early embryonic development. Mol Hum Reprod, 18:425-434.

Mucci N, Aller J, Kaiser GG, Hozbor F, Cabodevila J, Alberio RH. Effect of estrous cow serum during bovine embryo culture on blastocyst development and cryotolerance after slow freezing or vitrification. Theriogenology, 65:1551-1562.

Munoz M, Uyar A, Correia E, Diez C, Fernandez-Gonzalez A, Caamano JN, Martinez-Bello D, Trigal B, Humblot P, Ponsart C, Guyader-Joly C, Carrocera S, Martin D, Marquant Le Guienne B, Seli E, Gomez E. 2014. Prediction of pregnancy viability in bovine in vitro-produced embryos and recipient plasma with Fourier transform infrared spectroscopy. J Dairy Sci, 97:5497-5507.

Nagai K, Yanagawa Y, Katagiri S, Nagano M. 2015. Fertilizability of oocytes derived from Holstein cows having different antral follicle counts in ovaries. Anim Reprod Sci, 163:172-178.

Nagano M. 2019. Acquisition of developmental competence and in vitro growth culture of bovine oocytes. J Reprod Dev, in press.

Nedambale TL, Dinnyés A, Groenc W, Dobrinsky JR, Tiana XC, Yanga X. 2004. Comparison on in vitro fertilized bovine embryoscultured in KSOM or SOF and cryopreservedby slow freezing or vitrification. Theriogenology, 62:437-449.

O’Kearney-Flynn M, Wade M, Duffy P, Gat V, Boland MP, Dobrinsky JR. 1998. Effect of cryopreservation on IVP cattle embryo development in vitro and in vivo. Theriogenology, 49:173

Overstrom EW, Duby RT, Dobrinsky JR, Robb JM, Baguisi A, Lonergan P. 1993. Cytoskeletal damage in vitrified or frozen bovine embryos. Theriogenology, 39:276.

Overström EW. 1996. In vitro assessment of embryo viability. Theriogenology, 45:3-16.

Paschoal DM, Sudano MJ, Guastali MD, Dias Maziero RR, Crocomo LF, Ona Magalhaes LC, da Silva Rascado T, Martins A, da Cruz Landim-Alvarenga F. 2014. Forskolin effect on the cryosurvival of in vitro-produced bovine embryos in the presence or absence of fetal calf serum. Zygote 22:146-157.

Pereira RM, Baptista MC, Vasques MI, Horta AE, Portugal PV, Bessa RJ, Silva JC, Pereira MS, Marques CC. 2007. Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t,12c CLA). Anim Reprod Sci, 98:293-301.

Pero ME, Zullo G, Esposito L, Iannuzzi A, Lombardi P, De Canditiis C, Neglia G, Gasparrini B. 2018. Inhibition of apoptosis by caspase inhibitor Z-VAD-FMK improves cryotolerance of in vitro derived bovine embryos. Theriogenology, 108:127-135.

Perry G. 2016 Statistics of embryo collection and transfer in domestic farm animals. International embryo technology society. 2017. Available from: Accessed in: May 10th. 2019.

Peterson AJ, Lee RS. 2003. Improving successful pregnancies after embryo transfer. Theriogenology, 59:687-97.

Phillips T. 2008. Non-coding RNA and Gene Expression. Nature Education, 1:115.

Ralston A, Rossant J. 2008. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol, 313:614-629.

Ramos-Ibeas P, Heras S, Gómez-Redondo I, Planells B, Fernández-González R, Pericuesta E, Laguna-Barraza R, Pérez-Cerezales S, Gutiérrez-Adán A. 2019. Embryo responses to stress induced by assisted reproductive technologies. Mol Reprod Dev, 1-15.

Räty M, Ketoja E, Pitkänen T, Ahola V, Kananen K, Peippo J. 2011. In vitro maturation supplements affect developmental competence of bovine cumulus-oocyte complexes and embryo quality after vitrification. Cryobiology, 63:245-255.

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 Domest Anim, 43:44-50.

Rizos D, Ward F, Duffy P, Boland MP, 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.

Rodgaard T, Heegaard PM, Callesen H. 2015. Non-invasive assessment of in-vitro embryo quality to improve transfer success. Reprod Biomed Online, 31:585-592.

Salilew-Wondim D, Holker M, Rings F, Ghanem N, Ulas-Cinar M, Peippo J, Tholen E, Looft C, Schellander K, Tesfaye D. 2010. Bovine pretransfer endometrium and embryo transcriptome fingerprints as predictors of pregnancy success after transfer. Physiological Genomics, 42:201-218.

Sanches BV, Lunardelli PA, Tannura JH, Cardoso BL, Pereira MH, Gaitkoski D, Basso AC, Arnold DR, Seneda MM. 2016. A new direct transfer protocol for cryopreserved IVF embryos. Theriogenology, 85:1147-1151.

Sanches BV, Marinho LS, Filho BD, Pontes JH, Basso AC, Meirinhos ML, Silva-Santos KC, Ferreira CR, Seneda MM. 2013. Cryosurvival and pregnancy rates after exposure of IVF-derived bos indicus embryos to forskolin before vitrification. Theriogenology, 80:372-377.

Santos P, Chaveiro A, Simões N, Moreira da Silva F. 2008. Bovine oocyte quality in relation to ultrastructural characteristics of zona pellucida, polyspermic penetration and developmental competence. Reprod Domest Anim., 43:685-689.

Sata R, Tsujii H, Abe H, Yamashita S, Hoshi H. 1999. Fatty acid composition of bovine embryos cultured in serum-free and serum-containing medium during early embryonic development. J Reprod Dev, 45:97-103.

Schaefer AM, McFarland R, Blakely EL, He L, Whittaker RG, Taylor RW, Chinnery PF, Turnbull DM. 2008. Prevalence of mitochondrial DNA disease in adults. Ann Neurol, 63:35-39.

Schatten H, Sun QY, Prather R. 2014. The impact of mitochondrial function/dysfunction on IVF and new treatment possibilities for infertility. Reprod Biol Endocrinol, 12:111.

Schrode N, Xenopoulos P, Piliszek A, Frankenberg S, Plusa B, Hadjantonakis AK. 2013. Anatomy of a blastocyst: cell behaviors driving cell fate choice and morphogenesis in the early mouse embryo. Genesis, 51:219-233.

Sirard MA, Richard F, Blondin P, Robert C. 2006. Contribution of the oocyte to embryo quality. Theriogenology, 65:126-136.

Spikings EC, Alderson J, St John JC. 2006. Transmission of mitochondrial DNA following assisted reproduction and nuclear transfer. Hum Reprod Update, 12:401-415.

Spikings EC, Alderson J, St John JC. 2007. Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol Reprod, 76:327-335.

St John JC, Facucho-Oliveira J, Jiang Y, Kelly R, Salah R. 2010. Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Hum Reprod Update, 16:488-509.

Stephenson RO, Rossant J, Tam PP. 2012. Intercellular Interactions, Position, and Polarity in Establishing Blastocyst Cell Lineages and Embryonic Axes. Cold Spring Harb Perspect Biol, 4:a008235.

Sudano MJ, Caixeta ES, Paschoal DM, Martins A, Machado R, Buratini J, Landim-Alvarenga FDC.

2013a. Cryotolerance and global gene-expression patterns of Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts. Reprod Fertil Dev, 26:1129-1141.

Sudano MJ, Marinho LSR, Costa CB, Cancian R. 2016b. Cryopreservation of Bovine Embryos. In: Seneda MM, Silva-Santos KC, Marinho LSR (Ed.). Biotechnology of Animal Reproduction. Hauppauge, NY, USA: Nova Science Publishers. p.1-33

Sudano MJ, Marinho LSR, Silveira JC, Basso AC, Bohrer R, Lamberti GSE, Watanabe YF, Seneda MM, Meirelles FV. Evolução aplicada da produção in vitro de embriões bovinos. In Gonçalves PBD, Figueiredo JR, Gasperin BG. (Ed.) Biotécnicas aplicadas à reprodução animal, 2019, 3 ed. Grupo Gen, in press.

Sudano MJ, Paschoal DM, da Silva Rascado T, Magalhães LCO, Crocomo LF, de Lima-Neto JF, da Cruz Landim-Alvarenga F. 2011. Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology, 75:1211-1220.

Sudano MJ, Paschoal DM, Maziero RRD, Rascado TS, Guastali MD, Crocomo LF, Magalhães LCO, Monteiro BA, Martins Jr A, Machado R, Landim-Alvarenga FDC. 2013b. Improving postcryopreservation curvival capacity: an embryo-focused approach. Anim Reprod, 10:160-167

Sudano MJ, Rascado TD, Tata A, Belaz KR, Santos VG, Valente RS, Mesquita FS, Ferreira CR, Araujo JP, Eberlin MN, Landim-Alvarenga FD. 2016a. Lipidome signatures in early bovine embryo development. Theriogenology, 86:472-484.

Sudano MJ, Santos VG, Tata A, Ferreira CR, Paschoal DM, Machado R, Buratini J, Eberlin MN, Landim-Alvarenga FDC. 2012. Phosphatidylcholine and Sphingomyelin Profiles Vary in Bos taurus indicus and Bos taurus taurus In Vitro- and In Vivo-Produced Blastocysts. Biol Reprod, 87:1-11.

Tan K, An L, Wang SM, Wang XD, Zhang ZN, Miao K, Sui LL, He SZ, Nie JZ, Wu ZH, Tian JH. 2015. Actin Disorganization Plays a Vital Role in Impaired Embryonic Development of In Vitro-Produced Mouse Preimplantation Embryos. PLoS One, 10:e0130382.

Thompson JG, Brown HM, Sutton-McDowall ML. 2016. Measuring embryo metabolism to predict embryo quality. Reprod Fertil Dev, 28:41-50.

Thouas GA, Trounson AO, Jones GM. 2005. Effect of female age on mouse oocyte developmental competence following mitochondrial injury. Biol Reprod, 73:366-373.

Thouas GA, Trounson AO, Wolvetang EJ, Jones GM. 2004. Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol Reprod, 71:1936-1942.

Tripurani SK, Wee G, Lee KB, Smith GW, Wang L Jianboyao. 2013. MicroRNA-212 post-transcriptionally regulates oocyte-specific basic-helix-loop-helix transcription factor, factor in the germline alpha (FIGLA), during bovine early embryogenesis. PLoS One, 8:e76114.

Ushijima H, Yamakawa H, Nagashima H. 1999. Cryopreservation of bovine pre-morula-stage in vitro matured/in vitro fertilized embryos after delipidation and before use in nucleus transfer. Biol Reprod, 60:534-539.

Vajta G, Holm P, Kuwayama M, Booth PJ, Jacobsen H, Greve T, Callesen H. 1998. Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol Reprod Dev, 51:53-58. Vajta G, Hyttel P, Callesen H. 1997. Morphological changes of in-vitro-produced bovine blastocysts after vitrification, in-straw direct rehydration, and culture. Mol Reprod Dev, 48, 9-17.

Vajta G, Kuwayama M. 2006. Improving cryopreservation systems. Theriogenology, 65:236-244.

Van Blerkom J. 2004. Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction, 128:269-280.

Van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: Where they are and how they behave. Nat Rev Mol Cell Biol, 9:112-124.

Van Soom A, Boerjan M, Ysebaert MT, De Kruif A. 1996. Cell allocation to the inner cell mass and the trophectoderm in bovine embryos cultured in two different media. Mol Reprod Dev, 45:171-182.

Van Soom A, Mahmoudzadeh AR, Christophe A, Ysebaert MT, de Kruif A. 2001. Silicone oil used in microdrop culture can affect bovine embryonic development and freezability. Reprod Domest Anim, 36:169-176.

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, 7:664-670.

Van Soom A, Ysebaert MT, de Kruif A. 1997. Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol Reprod Dev, 47:47-56.

Van Wagtendonk-de Leeuw AM, den Daas JH, Rall WF. 1997. Field trial to compare pregnancy rates of bovine embryo cryopreservation methods: vitrification and one-step dilution versus slow freezing and three step dilution. Theriogenology, 48:1071-1084.

Van Wagtendonk-De Leeuw AM1, Den Daas JH, Kruip TA, Rall WF. 1995. Comparison of the efficacy of conventional slow freezing and rapid cryopreservation methods for bovine embryos. Theriogenology, 32:157-167.

Viana JH. 2018. A produção de embriões bovinos em 2017: o mercado em stand-by. Jornal o embrião, 62:6-10.

Wai T, Ao A, Zhang X, Cyr D, Dufort D, Shoubridge EA. 2010. The role of mitochondrial DNA copy number in mammalian fertility. Biol Reprod, 83:52-62.

Wakefield SL, Lane M, Mitchell M. 2011. Impaired mitochondrial function in the preimplantation embryo perturbs fetal and placental development in the mouse. Biol Reprod, 84:572-580.

Walker SK, Hartwich KM, Seamark RF. 1996. The production of unusually large offspring following embryo manipulation: Concepts and challenges. Theriogenology, 45:111-120.

Wang H, Dey SK. 2005. Lipid signaling in embryo implantation. Prostaglandins and Other Lipid Mediators, 77:84-102.

Ward F, Enright B, Rizos D, Boland M, Lonergan P. 2002. Optimization of in vitro bovine embryo production: effect of duration of maturation, length of gamete co-incubation, sperm concentration and sire. Theriogenology, 57:2105-2117.

Warzych E, Wrenzycki C, Peippo J, Lechniak D. 2007. Maturation medium supplements affect transcript level of apoptosis and cell survival related genes in bovine blastocysts produced in vitro. Mol Reprod Dev, 74:280-289.

Whittingham D, Leibo S, Mazur P. 1972. Survival of mouse embryos frozen to-196 and-269 C. Science, 178:411-414.

Wrenzycki C, Stinshoff H. 2013. Maturation environment and impact on subsequent developmental competence of bovine oocytes. Reprod Domest Anim, 48:38-43.

Xu J, Guo Z, Su L, Nedambale TL, Zhang J, Schenk J, Moreno JF, Dinnyes A, Ji W, Tian XC, Yang X, Du F. 2006. Developmental potential of vitrified holstein cattle embryos fertilized in vitro with sex-sorted sperm. J Dairy Sci, 89:2510-2518.

Yu XL, Deng W, Liu FJ, Li YH, Li XX, Zhang YL, Zan LS. 2010. Closed pulled straw vitrification of in vitro-produced and in vivo-produced bovine embryos. Theriogenology, 73:474-479.

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