Cryopreservation of in vitro-produced embryos: challenges for commercial implementation
Bruno Valente Sanches, Amanda Fonseca Zangirolamo, Nathalia Covre da Silva, Fabio Morotti, Marcelo Marcondes Seneda
Abstract
In the last several years, the high demand for embryo production has resulted in the need to study new methods to make the cryopreservation of bovine embryos produced in vitro more efficient. Despite the advantages offered by in vitro embryo production (IVEP), the major challenge to its greater dissemination is to improve embryonic survival after cryopreservation. Embryos that are produced in vitro are less resistant to cryopreservation compared to those produced in vivo, which is due to the higher accumulation of lipids in their cells, among other factors. In this context, changes in the culture conditions such as the addition of lipolytic chemical substances and the adjustment of fetal calf serum in the medium have been proposed to decrease the lipid amount within the embryos. Several years ago, vitrification allowed good results for in vitro produced (IVP) embryos because of its simplicity, speed and low cost. More recently, another technique applied to simplify the embryo post-thawing rehydration step in vivo, direct transfer (DT), is a strategy that has proven to be of interest in helping to overcome limitations to the cryopreservation of in vitro produced embryos. DT has been performed by commercial laboratories, ensuring good embryo viability after thawing. However, commercial and operational limitations prevent the large-scale use of these techniques. Thus, this review aims to discuss the use of strategies to improve the postcryopreservation survival capacity and the aspects to be overcome so that the cryopreservation of IVP embryos becomes a well-established and commercially applicable technique in addition to presenting new guidelines for embryo transfer (ET) programs from a better selection of recipients.
Keywords
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 serumcontaining media. Mol Reprod, 61:57-66.
Andrade GA, Fernandes MA, Knychala RM, Pereira Junior MV, Oliveira AJ, Nunes DP, Bonato G, Santos RM. 2012. Fatores que afetam a taxa de prenhez de receptoras de embriões bovinos produzidos in vitro. Rev Bras Reprod Anim, 36:66-69.
Baguisi A, Lonergan P, Overstrom E, Boland M. 2000. Vitrification of bovine embryos: incidence of necrosis and apoptosis. Theriogenology, 55:162.Abstract. Barceló-Fimbres M, Seidel GEJ. 2007a. Effects of either glucose or fructose and metabolic regulators on bovine embryo development and lipid accumulation in vitro. Mol Reprod Dev, 74:1406-1418.
Barceló-Fimbres M, Seidel GEJ. 2007b. 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.
Callesen H, Liboriussen T, Greve T. 1996. Practical aspects of multiple ovulation-embryo transfer in cattle. Anim Reprod Sci, 42:205-214.
Chebel RC, Demétrio DGB, Metzger J. 2008. Factor affecting success of embryo collection and transfer in large dairy herds. Theriogenology, 69: 98-106.
Crosier AE, Farin PW, Dykstra MJ, Alexander JE, Farin CE. 2001. Ultrastructural morphometry of bovine blastocysts produced in vivo or in vitro. Biol Reprod, 64:1375-1385.
Dairy Herd Management [homepage on the Internet]. 2017. The genomics of fertility and health traits. Available on: http://www.dairyherd.com/advice-andtips/reproduction/genomics-fertility-and-health-traits. Accessed on: April 10,. 2017.
De La Torre-Sanchez JF, Gardner DK, Preis K, Gibbons J, Seidel GE. 2006. Metabolic regulation of in vitro-produced bovine embryos. II. Effects of phenazine ethosulfate, sodium azide and 2,4-dinitrophenol during post-compaction development on glucose metabolism and lipid accumulation. Reprod Fertil Dev, 18:597-607.
Dode MAN, Leme LO, Spricigo JFW. 2013. Criopreservação de embriões bovinos produzidos in vitro. Rev Bras Reprod Anim, 37:145-150.
Farin CE, Farin PW, Piedrahita JA. 2004. Development of fetuses from in vitro-produced and cloned bovine embryos. J Anim Sci, 82(E-suppl):53-62. Ferreira G. 2013. Reproductive performance of dairy farms in western Buenos Aires province, Argentina. J Dairy Sci, 96:8075-8080.
Feugang JM, Camargo-Rodriguez O, Memili E. 2009. Culture systems for bovine embryos. Livest Sci, 121:141-149.
Gad A, Hoelker M, Besenfelder U, Havlicek V, Cinar U, Rings F, Held E, Dufort I, Sirard MA, Schellander K, Tesfaye D. 2012. Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol Reprod, 87:100. doi: 10.1095/biolreprod.112.099697.
Gardner DK. 2008. Dissection of culture media for embryos: the most important and less important components and characteristics. Reprod Fertil Dev, 20:9-18.
Hasler JF, Mccauley AD, Lathrop WF, Foote RH. 1987. Effect of donor-embryo-recipient interactions on pregnancy rate in a large-scale bovine embryo transfer program. Theriogenology, 27:139-168.
Hasler JF. 2010. Synthetic media for culture, freezing and vitrification of bovine embryos. Reprod Fertil Dev, 22:119-125.
Jones AL, Lamb GC. 2008. Nutrition, synchronization, and management of beef embryo transfer recipients. Theriogenology, 69:107-115.
Kocyigit A, Cevik M. 2016. Correlation between the cryosurvival, cell number and diameter in bovine in vitro produced embryos. Cryobiology, 73: 203-208.
Kuwayama M, Vajta G, Kato O, Leibo SP. 2005. Highly efficient vitrification method for cryopreservation of human oocytes. Reprod Biomed, 11:300-308.
Lane M, Schoolcraft WB, Gardner DK. 1999. Vitrification of mouse and human blastocysts using a novel cryoloop container-less technique. Fertil Steril, 72:1073-1078.
Leroy JL, Opsomer G, De Vliegher S, Vanholder T, Goossens L, Geldhof A, Bols PE, DE Kruif A, Van Soom A. 2005. Comparison of embryo quality in highyielding dairy cows, in dairy heifers and in beef cows. Theriogenology, 64:2022-2036.
Marinho LSR, Untura RM, Morotti F, Moino LL, Rigo AG, Sanches BV, Pontes JHF, Seneda MM. 2012. Large-scale programs for recipients of in vitroproduced embryos. Anim Reprod, 9:323-328.
Marinho LSR, Sanches BV, Rosa CO, Tannura JH, Rigo AG, Basso AC, Pontes JHF, Seneda MM. 2015. Pregnancy rates to fixed embryo transfer of vitrified IVP Bos indicus, Bos Taurus or Bos indicus x Bos taurus embryos. Reprod Domest Anim, 50:807-811.
Márquez-Alvarado YC, Galina CS, Castilla B, León H, Moreno-Mendoza N. 2004. Evidence of damage in cryopreserved and fresh bovine embryos using the TUNEL technique. Reprod Domest Anim, 39:141-145.
McKeegan PJ, Sturmey RG. 2012. The role of fatty acids in oocyte and early embryo development. Reprod Fertil Dev, 24:59-67.
Men H, Agca Y, Riley LK, Critser JK. 2006. Improved survival of vitrified porcine embryos after partial delipation through chemically stimulated lipolysis and inhibition of apoptosis. Theriogenology, 66:2008-2016.
Moore K, Rodriguez-Sallaberry CJ, Kramer JM, Johnson S, Wroclawska,E, Goicoa S, Niasari-Naslaji A. 2007. In vitro production of bovine embryos in medium supplemented with a serum replacer: effects on blastocyst development, cryotolerance and survival to term. Theriogenology, 68:1316-1325.
Morotti F, Sanches BV, Pontes JHF, Basso AC, Siqueira ER, Lisboa LA, Seneda MM. 2014. Pregnancy rate and birth rate of calves from a largescale IVF program using reverse-sorted semen in Bos indicus, Bos indicus-taurus, and Bos taurus cattle. Theriogenology, 81:696-701.
Mucci N, Aller J, Kaiser GG, Hozbor F, Cabodevila J, Alberio RH. 2006. Effect of estrous cow serum during bovine embryo culture on blastocyst development and cryotolerance after slow freezing or vitrification. Theriogenology, 65:1551-1562.
Overstrom EW. 1996. In vitro assessment of embryo viability. Theriogenology, 45:3-16.
Papis K, Shimizu M, Izaike Y. 2000. Factors affecting the survivability of bovine oocytes vitrified in droplets. Theriogenology, 54:651-658.
Park SY, Kim EY, Cui XS, Tae JC, Lee WD, Kim NH, Park SP, Lim JH. 2006. Increase in DNA fragmentation and apoptosis-related gene expression in frozen–thawed bovine blastocysts. Zygote, 14:125-131.
Paschoal DM, Sudano MJ, Schwarz KRL, Maziero RRD, Guastali MD, Crocomo LF, Magalhães LCO, Martins Jr, A, Leal ALV, Landim-Alvarenga FC. 2017. Cell apoptosis and lipid content of in vitro– produced, vitrified bovine embryos treated with forskolin. Theriogenology, 87:108-114.
Peixoto MGCD, Bergmann JAG, Alvim MTT, Penna VM. 2004. Fatores que influenciaram a prenhez de embriões zebuínos em receptoras mestiças. In: Abstracts of the V Simpósio da Sociedade Brasileira de Melhoramento Animal, 2004, Pirassununga, SP. Pirassununga, SP: SBMA. 4 pp.
Pereira RM, Marques CC. 2008. Animal oocyte and embryo cryopreservation. Cell Tissue Bank, 9:267-277. Perry G. 2016. IETS 2016. 2015 Statistics of embryo collection and transfer in domestic farm animals. Embryo Technology Newsletter, 34: 1-75.
Pollard JW, Leibo SP. 1994. Chilling sensitivity of mammalian embryos. Theriogenology, 41:101-106.
Pontes JHF, Silva KCF, Basso AC, Rigo AG, Ferreira CR, Santos GMG, Sanches, BV, Porcionato, JPF, Vieira, PHS, Faifer, FS, Sterza, FAM, Schenkd, JL, Seneda, MM. 2010. Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus-taurus dairy cows using sexed sperm. Theriogenology, 74:1349-1355.
Pontes JHF, Melo Sterza FA, Basso AC, Ferreira CR, Sanches BV, Rubin KC, Seneda MM. 2011. Ovum pick up, in vitro embryo production, and pregnancy rates from a large-scale commercial program jusing Nelore cattle (Bos indicus) donors. Theriogenology, 75:1640-1646.
Pryor JH, Trant JA, Ponchirolli-Schneider CB, Looney CR, Long CR, Forrest DW. 2009. The use of forskolin and its effect on in vitro-produced brahmansired embryos submitted to slow cool freezing or vitrification. Reprod Fertil Dev, 22:214-214.
Randi F, Fernandez-Fuertes B, McDonald M, Forde N, Kelly AK, Amorin HB, Lima EM, Morotti F, Seneda MM, Lonergan P. 2015. Asynchronous embryo transfer as a tool to understand embryo–uterine interaction in cattle: is a large conceptus a good thing? Reprod Fertil Dev, 28:1999-2006.
Sanches BV, Marinho LSR, Filho BDO, Pontes JHF, Basso AC, Meirinhos, MLG, 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.
Sanches BV, Lunardelli PA, Tannura JH, Cardoso BL, Pereira MHC, Gaitkoski G, Basso AC, Arnold DR, Seneda MM. 2016. A new direct transfer protocol for cryopreserved IVF embryos. Theriogenology, 85:1147-1151.
Saragusty J, Arav A. 2011. Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction, 141: 1-19.
Segerson EC, Hansen TR, Libby DW, Randel RD, Getz WR. 1984. Ovarian and uterine morphology and function in Angus and Brahman cows. J Anim Sci, 59:1026-1046.
Silva-Santos KC, Santos GMG, Siloto LS, Hertel MF, Andrade ER, Rubin MIB, Sturion L, MeloSterza FA, Seneda MM. 2011. Estimate of the population of preantral follicles in the ovaries of Bos taurus indicus and Bos taurus taurus cattle. Theriogenology, 76:1051-1057.
Sreenan JM, Diskin MG. 1987. Factors affecting pregnancy rate following embryo transfer in the cow. Theriogenology, 27:99-113.
Stewart BM, Block J, Morelli P, Navarette AE, Amstalden M, Bonilla L, Hansen PJ, Bilby TR. 2011. Efficacy of embryo transfer in lactating dairy cows during summer using fresh or vitrified embryos produced in vitro with sex-sorted semen. J Dairy Sci, 94:3437-3445.
Stroud B. 2011. IETS 2011 Statistics and data retrieval committee report: the year 2010 worldwide statistics of embryo transfer in domestic farm animals. Embryo Trans Newslett, 29:14–23.
Stroud B. 2012. IETS 2012 statistics and data retrieval committee report: the year 2011 world wide statistics of embryo transfer in domestic farm animals. Embryo Trans Newslett, 30:16-26.
Sudano MJ, Paschoal DM, Rascado TD, Magalhaes LCO, Crocomo LF, Lima-Neto JF, LandimAlvarenga FD. 2011. Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology, 75:1211- 1220.
Sudano MJ, Santos VG, Tata A, Ferreira CR, Paschoal DM, Machado R, Buratini J, Eberlin MN, Landim-Alvarenga FDC. 2012b. 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. doi: 10.1095/biolreprod.112.102897.
Sudano MJ, Paschoal DM, Maziero RRD, Rascado TS, Guastali MD, Crocomo LF, Magalhães LCO, Monteiro BA, Martins Jr A, Machado R, LandimAlvarenga FDC. 2013. Improving postcryopreservation survival capacity: an embryo-focused approach. Anim. Reprod, 10:160-167.
Sudano MJ, Paschoal DM, Rascado TS, Crocomo LF, Magalhaes LC, Junior AM, Machado R, Landim-Alvarenga FC. 2012a. Crucial surviving aspects for vitrified in vitro-produced bovine embryos. Zygote, 22:124-131.
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, Kuwayama M. 2006. Improving cryopreservation systems. Theriogenology, 65:236-244. Viana JHM. 2012. Levantamento estatístico da produção de embriões bovinos no Brasil em 2011: mudanças e tendências futuras. O Embrião, 51:6-10.
Visintin JA, Martins JFP, Bevilacqua EM, Mello MRB, Nicácio AC, Assumpção MEOA. 2002. Cryopreservation of Bos taurus vs. Bos indicus embryos: are they really different? Theriogenology, 57:345-359.
Voelkel SA, Hu YX. 1992. Direct transfer of frozenthawed bovine embryos. Theriogenology, 37:23-37.