Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0022
Animal Reproduction (AR)
Conference Paper

From reproductive technologies to genome editing in small ruminants: an embryo’s journey

Alejo Menchaca, Pedro C. dos Santos-Neto, Frederico Cuadro, Marcela Souza-Neves, Martina Crispo

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Abstract

The beginning of this century has witnessed great advances in the understanding of ovarian physiology and embryo development, in the improvement of assisted reproductive technologies (ARTs), and in the arrival of the revolutionary genome editing technology through zygote manipulation. Particularly in sheep and goats, the current knowledge on follicular dynamics enables the design of novel strategies for ovarian control, enhancing artificial insemination and embryo production programs applied to genetic improvement. In vitro embryo production (IVEP) has evolved due to a better understanding of the processes that occur during oocyte maturation, fertilization and early embryo development. Moreover, interesting advances have been achieved in embryo and oocyte cryopreservation, thereby reducing the gap between the bench and on-farm application of IVEP technology. Nevertheless, the major breakthrough of this century has been the arrival of the CRISPR/Cas system for genome editing. By joining diverse disciplines such as molecular biology, genetic engineering and reproductive technologies, CRISPR allows the generation of knock-out and knock-in animals in a novel way never achieved before. The innumerable applications of this disruptive biotechnology are challenging the imagination of those who intend to build the animals of the future.

Keywords

cryopreservation, genome modification, IVF, MOET, ovine, transgenesis.

References

Arav A. 2014. Cryopreservation of oocytes and embryos. Theriogenology, 81:96-102.

Baguisi A, Behboodi E, Melican DT, Pollock JS, Destrempes MM, Cammuso C, Williams JL, Nims SD, Porter CA, Midura P, Palacios MJ, Ayres SL, Denniston RS, Hayes ML, Ziomek CA, Meade HM, Godke RA, Gavin WG, Overstrom EW, Echelard Y. 1999. Production of goats by somatic cell nuclear transfer. Nat Biotechnol, 17:456-461.

Balaro MFA, Fonseca JF, Barbosa TGB, Souza-Fabjan JMG, Figueira LM, Teixeira TA, Carvalheira LR, Brandão FZ. 2016. Potential role for GnRH in the synchronization of follicular emergence before the superovulatory DAY 0 protocol. Domest Anim Endocrinol, 54:10-14.

Baldassarre H, Furnus CC, De Matos DG, Pessi H. 1996. In vitro production of sheep embryos using laparoscopic folliculocentesis: alternative gonadotrophin treatments for stimulation of oocyte donors. Theriogenology, 45:707-717.

Baldassarre H, Wang B, Kafidi N, Keefer C, Lazaris A, Karatzas CN. 2002. Advances in the production and propagation of transgenic goats using laparoscopic ovum pick-up and in vitro embryo production technologies. Theriogenology, 57:275-284.

Baldassarre H, Keefer C, Wang B, Lazaris A, Karatzas CN. 2003a. Nuclear transfer in goats using in vitro matured oocytes recovered by laparoscopic ovum pick-up. Cloning Stem Cells, 5:279-285.

Baldassarre H, Wang B, Kafidi N, Gauthier M, Neveu N, Lapointe J, Sneek L, Leduc M, Duguay F, Zhou JF, Lazaris A, Karatzas CN. 2003b. Production of transgenic goats by pronuclear microinjection of in vitro produced zygotes derived from oocytes recovered by laparoscopy. Theriogenology, 59:831-839.

Barrera N, dos Santos Neto PC, Cuadro F, Bosolasco D, Mulet AP, Crispo M and Menchaca A. 2018. Impact of delipidated estrous sheep serum suplementation on in vitro maturation, cryotolerance and endoplasmic reticulum stress gene expression of sheep oocytes. PLoS One. doi.org/10.1371/ journal.pone.0198742.

Bartlewski P M, Alexander BD, Rawlings NC, Barrett DMW, King WA. 2008. Ovarian responses, hormonal profiles and embryo yields in anoestrous ewes superovulated with Folltropin-V after pretreatment with medroxyprogesterone acetate-releasing vaginal sponges and a single dose of oestradiol-17β. Reprod Domest Anim, 43:299-307.

Bartlewski PM, Baby TE, Giffin JL. 2011. Reproductive cycles in sheep. Anim Reprod Sci, 124:259-268.

Bartlewski PM, Seaton P, Franco Oliveira ME, Kridli RT, Murawski M, Schwarz T. 2016. Intrinsic determinants and predictors of superovulatory yields in sheep: Circulating concentrations of reproductive hormones, ovarian status, and antral follicular blood flow. Theriogenology, 86:130-143.

Bevacqua RJ, Fernandez-Martin R, Canel NG, Gibbons A, Texeira D, Lange F, Vans Landschoot G, Savy V, Briski O, Hiriart MI, Grueso E, Ivics Z, Taboga O, Kues WA, Ferraris S, Salamone DF. 2017. Assessing Tn5 and sleeping beauty for transpositional transgenesis by cytoplasmic injection into bovine and ovine zygotes. PLoS One, 12:e0174025. doi.org/10.1371/journal.pone.0174025.

Campbell KHS. 2002. Transgenic sheep from cultured cells. In: Clarke AR (Ed.). Transgenesis Techniques: Principles and Protocols. Totowa, NJ: Springer. pp. 289-301.

Casali R, Pinczak A, Cuadro F, Guillen-Muñoz JM, Mezzalira A, Menchaca A. 2017. Semen deposition by cervical, transcervical and intrauterine route for fixed-time artificial insemination (FTAI) in the ewe. Theriogenology, 103:30-35.

Cognie Y, Baril G, Poulin N, Mermillod P. 2003. Current status of embryo technologies in sheep and goat. Theriogenology, 59:171-188.

Crispo M, Mulet AP, Tesson L, Barrera N, Cuadro F, Dos Santos-Neto PC, Nguyen TH, Creneguy A, Brusselle L, Anegon I, Menchaca A. 2015a. Efficient generation of myostatin knock-out sheep using CRISPR/Cas9 technology and microinjection into zygotes. PLoS One, 10:e0136690. doi: 10.1371/journal.pone.0136690.

Crispo M, Vilarino M, Dos Santos-Neto PC, Nunez-Olivera R, Cuadro F, Barrera N, Mulet AP, Nguyen TH, Anegon I, Menchaca A. 2015b. Embryo development, fetal growth and postnatal phenotype of eGFP lambs generated by lentiviral transgenesis. Transgenic Res, 24:31-41.

Dattena M, Ptak G, Loi P, Cappai P. 2000. Survival and viability of vitrified in vitro and in vivo produced ovine blastocysts. Theriogenology, 53:1511-1519.

Deng S, Li G, Zhang J, Zhang X, Cui M, Guo Y, Liu G, Li G, Feng J, Lian Z. 2013.Transgenic cloned sheep overexpressing ovine toll-like receptor 4. Theriogenology, 80:50-57.

Evans ACO. 2003. Ovarian follicle growth and consequences for fertility in sheep. Anim Reprod Sci, 78:289-306.

Ferreira-Silva JC, Moura MT, Silva TD, Oliveira LRS, Chiamenti A, Figueirêdo Freitas VJ, Oliveira MAL. 2017. Full-term potential of goat in vitro produced embryos after different cryopreservation methods. Cryobiology, 75:75-79.

Fonseca JF, Bruschi JH, Santos ICC, Viana JHM, Magalhães ACM. 2005. Induction of estrus in non-lactating dairy goats with different estrous synchrony protocols. Anim Reprod Sci, 85:117-124.

Fonseca JF, Souza-Fabjan JMG, Oliveira MEF, Cruz RC, Esteves LV, Matos de Paiva MPSL, Brandão FZ, Mancio AB. 2017. Evaluation of cervical mucus and reproductive efficiency of seasonally anovular dairy goats after short-term progestagen-based estrous induction protocols with different gonadotropins. Reprod Biol, 17:363-369.

Frock RL, Hu J, Meyers RM, Ho YJ, Kii E, Alt FW. 2015. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat Biotechnol, 33:179-186.

Gao Y, Wu H, Wang Y, Liu X, Chen L, Li Q, Cui C, Liu X, Zhang J, Zhang Y. 2017. Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biol, 18(1):13. doi: 10.1186/s13059-016-1144-4.

Gibbons A, Pereyra Bonnet F, Cueto MI, Catala M, Salamone DF, Gonzalez-Bulnes A. 2007. Procedure for maximizing oocyte harvest for in vitro embryo production in small ruminants. Reprod Domest Anim, 42:423-426.

Gibbons A, Cueto MI, Pereyra Bonnet F. 2011. A simple vitrification technique for sheep and goat embryo cryopreservation. Small Rumin Res, 95:61-64.

Gonzalez-Bulnes A, Baird DT, Campbell BK, Cocero MJ, Garcia-Garcia RM, Inskeep EK, Lopez-Sebastian A, McNeilly AS, Santiago-Moreno J, Souza CJ, Veiga-Lopez A. 2004. Multiple factors affecting the efficiency of multiple ovulation and embryo transfer in sheep and goats. Reprod Fertil Dev, 16:421-435.

Hashimoto M, Yamashita Y, Takemoto T. 2016. Electroporation of Cas9 protein/sgRNA into early pronuclear zygotes generates non-mosaic mutants in the mouse. Dev Biol, 418:1-9.

Keefer CL, Baldassarre H, Keyston R, Wang B, Bhatia B, Bilodeau AS, Zhou JF, Leduc M, Downey BR, Lazaris A, Karatzas CN. 2001. Generation of dwarf goat (Capra hircus) clones following nuclear transfer with transfected and nontransfected fetal fibroblasts and in vitro-matured oocytes. Biol Reprod, 64:849-856.

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

Ledda S, Bogliolo L, Succu S, Ariu F, Bebbere D, Leoni GG, Naitana S. 2007. Oocyte cryopreservation: oocyte assessment and strategies for improving survival. Reprod Fertil Dev, 19:13-23.

Li H, Wang G, Hao Z, Zhang G, Qing Y, Liu S, Qing L, Pan W, Chen L, Liu G, Zhao R, Jia B, Zeng L, Guo J, Zhao L, Zhao H, Lv C, Xu K, Cheng W, Li H, Zhao HY, Wang W, Wei HJ. 2016. Generation of biallelic knock-out sheep via gene-editing and somatic cell nuclear transfer. Sci Rep, 6:33675. doi: 10.1038/srep33675.

Lima JTM, Fonseca JF, Balaro MFA, Esteves LV, Ascoli FO, Leite CR, Ribeiro ACS, Delgado KF, Souza-Fabjan JMG, Filho RAT, Brandão FZ. 2016. Effect of natural mating or laparoscopic artificial insemination in superovulated Santa Inês ewes on superovulatory response, fertility and embryo viability. Anim Prod Sci, 56:1463-1468.

Martínez AG, Valcárcel A, Furnus CC, de Matos DG, Iorio G, de las Heras MA. 2006. Cryopreservation of in vitro-produced ovine embryos. Small Rumin Res, 63:288-296.

Martins LT, Neto SG, Tavares KC, Calderón CE, Aguiar LH, Lazzarotto CR, Ongaratto FL, Rodrigues VH, Carneiro IdeS, Rossetto R, Almeida AP, Fernandes CC, Rondina D, Dias AC, Chies JM, Polejaeva IA, Rodrigues JL, Forell F, Bertolini LR, Bertolini M. 2016. Developmental outcome and related abnormalities in goats: Comparison between SCNT and in vivo-derived concepti during pregnancy through term. Cell Reprogram, 18:264-279.

Massip A. 2001. Cryopreservation of embryos of farm animals. Reprod Domest Anim, 36:49-55.

Menchaca A, Pinczak A, Rubianes E. 2002. Follicular recruitment and ovulatory response to FSH treatment initiated on day 0 or day 3 postovulation in goats. Theriogenology, 58:1713-1721.

Menchaca A, Rubianes E. 2004. New treatments associated with timed artificial insemination in small ruminants. Reprod Fertil Dev, 16:403-413.

Menchaca A, Rubianes E. 2007. Pregnancy rate obtained with short-term protocol for timed artificial insemination in goats. Reprod Domest Anim, 42:590-593.

Menchaca A, Miller V, Salveraglio V, Rubianes E. 2007a. Endocrine, luteal and follicular responses after the use of the Short-Term Protocol to synchronize ovulation in goats. Anim Reprod Sci, 102:76-87.

Menchaca A, Vilariño M, Crispo M, Pinczak A, Rubianes E. 2007b. Day 0 protocol: superstimulatory treatment initiated in the absence of a large follicle improves ovarian response and embryo yield in goats. Theriogenology, 68:1111-1117.

Menchaca A, Vilariño M, Pinczak A, Kmaid S, Saldana JM. 2009. Progesterone treatment, FSH plus eCG, GnRH administration, and Day 0 Protocol for MOET programs in sheep. Theriogenology, 72:477-483.

Menchaca A, Vilariño M, Crispo M, de Castro T, Rubianes E. 2010. New approaches to superovulation and embryo transfer in small ruminants. Reprod Fertil Dev, 22:113-118.

Menchaca A, Anegon I, Whitelaw CB, Baldassarre H, Crispo M. 2016a. New insights and current tools for genetically engineered (GE) sheep and goats. Theriogenology, 86:160-169.

Menchaca A, Barrera N, dos Santos-Neto PC, Cuadro F, Crispo M. 2016b. Advances and limitations of in vitro embryo production in sheep and goats. Anim Reprod, 13:273-278.

Menchaca A, Cuadro F, dos Santos-Neto PC, Bosolasco D, Barrera N, de Brun V, Crispo M. 2018. Oocyte developmental competence is improved by high progesterone concentrations during preovulatory follicular growth. Anim Reprod Sci. doi: 10.1016/j.anireprosci.2018.06.010.

Mogase CR, Lehloenya KC, Dattena M. 2016. Applicability of day 0 superovulation protocol in Boer goats. Small Rumin Res, 136:261-264.

Morató R, Romaguera R, Izquierdo D, Paramio MT, Mogas T. 2011. Vitrification of in vitro produced goat blastocysts: effects of oocyte donor age and development stage. Cryobiology, 63:240-244.

Nakade S, Yamamoto T, Sakuma T. 2017. Cas9, Cpf1 and C2c1/2/3-What's next? Bioengineered, 8:265-273.

Papadopoulos S, Rizos D, Duffy P, Wade M, Quinn K, Boland MP, Lonergan P. 2002. Embryo survival and recipient pregnancy rates after transfer of fresh or vitrified, in vivo or in vitro produced ovine blastocysts. Anim Reprod Sci, 74:35-44.

Paramio MT, Izquierdo D. 2016. Recent advances in in vitro embryo production in small ruminants. Theriogenology, 86:152-159.

Pereyra-Bonnet F, Gibbons A, Cueto M, Sipowicz P, Fernandez-Martin R, Salamone D. 2011. Efficiency of sperm-mediated gene transfer in the ovine by laparoscopic insemination, in vitro fertilization and ICSI. J Reprod Dev, 57:188-196.

Remy S, Chenouard V, Tesson L, Usal C, Ménoret S, Brusselle L, Heslan J-M, Nguyen TH, Bellien J, Merot J, De Cian A, Giovannangeli C, Concordet J-P, Anegon I. 2017. Generation of gene-edited rats by delivery of CRISPR/Cas9 protein and donor DNA into intact zygotes using electroporation. Sci Rep, 7:16554. doi:10.1038/s41598-017-16328-y.

Rubianes E, Menchaca A. 2003. The pattern and manipulation of ovarian follicular growth in goats. Anim Reprod Sci, 78:271-287.

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

Santos-Neto PC, García-Pintos C, Pinczak A, Menchaca A. 2015a. Fertility obtained with different progestogen intravaginal devices using short-term protocol for fixed-time artificial insemination (FTAI) in sheep. Livest Sci, 182:125-128.

Santos-Neto PC, Vilarino M, Barrera N, Cuadro F, Crispo M, Menchaca A. 2015b. Cryotolerance of Day 2 or Day 6 in vitro produced ovine embryos after vitrification by cryotop or Spatula methods. Cryobiology, 70:17-22.

Santos-Neto PC, Cuadro F, Barrera N, Crispo M, Menchaca A. 2017. Embryo survival and birth rate after minimum volume vitrification or slow freezing of in vivo and in vitro produced ovine embryos. Cryobiology, 78:8-14.

Schnieke AE, Kind AJ, Ritchie WA, Mycock K, Scott AR, Ritchie M, Wilmut I, Colman A, Campbell KH. 1997. Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science, 278:2130-2133.

Seidel GE Jr. 2006. Modifying oocytes and embryos to improve their cryopreservation. Theriogenology, 65:228-235.

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

Souza-Fabjan JMG, da Rosa RM, Balaro MFA, Pinto PHN, dos Santos GB, Arashiro EKN, da Fonseca JF, Ungerfeld R, Brandão FZ. 2017. Effect of different hormonal combinations on follicular wave emergence and superovulatory response in sheep. Theriogenology, 103:24-29.

Succu S, Bebbere D, Bogliolo L, Ariu F, Fois S, Leoni GG, Berlinguer F, Naitana S, Ledda S. 2008. Vitrification of in vitro matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance. Mol Reprod Dev, 75:538-546.

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

Taşdemir U, Ağaoğlu AR, Kaymaz M, Karakaş K. 2011. Ovarian response and embryo yield of Angora and Kilis goats given the day 0 protocol for superovulation in the non-breeding season. Trop Anim Health Prod, 43:1035-1038.

Teixeira PPM, Padilha LC, Oliveira MEF, Motheo TF, da Silva ASL, Barros FFPC, Coutinho LN, Flôres FN, Lopes MCS, Bandarra MB, Silva MAM, Vasconcelos RO, Rodrigues LFS, Vicente WRR. 2011. Laparoscopic ovum collection in sheep: Gross and microscopic evaluation of the ovary and influence on ooctye production. Anim Reprod Sci, 127:169-175.

Thompson JG, Mitchell M, Kind KL. 2007. Embryo culture and long-term consequences. Reprod Fertil Dev, 19:43-52.

Traldi AS, Leboeuf B, Cognié Y, Poulin N, Mermillod P. 1999. Comparative results of in vitro and in vivo survival of vitrified in vitro produced goat and sheep embryos. Theriogenology, 51:175. doi: 10.1016/S0093-691X(99)91734-X.

Travis J. 2015. Making the cut. Science, 350:1456-1457. Tsang WH, Chow KL. 2009. Mouse embryo cryopreservation utilizing a novel high-capacity vitrification spatula. Biotechniques, 46:550-552.

Ungerfeld R, Rubianes E. 1999. Effectiveness of short-term progestogen primings for the induction of fertile oestrus with eCG in ewes during late seasonal anoestrus. Anim Sci, 68:349-353.

Vajta G. 2000. Vitrification of the oocytes and embryos of domestic animals. Anim Reprod Sci, 60/61:357-364.

Vartak SV, Raghavan SC. 2015. Inhibition of nonhomologous end joining to increase the specificity of CRISPR/Cas9 genome editing. FEBS J, 282:4289-4294.

Veiga-Lopez A, Gonzalez-Bulnes A, Garcia-Garcia RM, Dominguez V, Cocero MJ. 2005. The effects of previous ovarian status on ovulation rate and early embryo development in response to superovulatory FSH treatments in sheep. Theriogenology, 63:1973-1983.

Vilariño M, Rubianes E, van Lier E, Menchaca A. 2010. Serum progesterone concentrations, follicular development and time of ovulation using a new progesterone releasing device (DICO®) in sheep. Small Rumin Res, 91:219-224.

Vilariño M, Rubianes E, Menchaca A. 2011. Re-use of intravaginal progesterone devices associated with the Short-term Protocol for timed artificial insemination in goats. Theriogenology, 75:1195-1200.

Vilariño M, Rubianes E, Menchaca A. 2013. Ovarian responses and pregnancy rate with previously used intravaginal progesterone releasing devices for fixed-time artificial insemination in sheep. Theriogenology, 79:206-210.

Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 153:910-918.

Wang X, Yu H, Lei A, Zhou J, Zeng W, Zhu H, Dong Z, Niu Y, Shi B, Cai B, Liu J, Huang S, Yan H, Zhao X, Zhou G, He X, Chen X, Yang Y, Jiang Y, Shi L, Tian X, Wang Y, Ma B, Huang X, Qu L, Chen Y. 2015. Generation of gene-modified goats targeting MSTN and FGF5 via zygote injection of CRISPR/Cas9 system. Sci Rep, 5:13878. doi:10.1038/srep13878.

Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature, 385:810-813.

Yu H, Chen J, Sun W, Liu S, Zhang A, Xu X, Wang X, He Z, Liu G, Cheng G. 2012. The dominant expression of functional human lactoferrin in transgenic cloned goats using a hybrid lactoferrin expression construct. J Biotechnol, 161:198-205.

Zhang P, Liu P, Dou H, Chen L, Chen L, Lin L, Tan P, Vajta G, Gao J, Du Y, Ma RZ. 2013. Handmade cloned transgenic sheep rich in omega-3 fatty acids. PLoS One, 8:e55941. doi.org/10.1371/journal.pone.0055941.

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