Postnatal consequences of assisted reproductive technologies in cattle
Peter J. Hansen, Luiz Gustavo B. Siqueira
Abstract
Experiments in mice and clinical observations in humans are indicative that adult phenotype can be altered in offspring derived from embryos that were subjected to culture or that were produced by the combination of in vitro oocyte maturation, fertilization and embryonic development (in vitro production; IVP). The most commonly observed changes are in body and organ size, growth rate, cardiovascular function and regulation of glucose homeostasis. In cattle, IVP is associated with increased birth weight and neonatal death loss but little is known about the long-term consequences of embryo technologies. Recently, postnatal characteristics were compared between females born as a result of artificial insemination, IVP using conventional semen, IVP using reverse X-sorted semen, and multiple ovulation – embryo transfer. Females born following IVP using reverse X-sorted semen produced less milk, milk fat, and milk protein than females in the other three groups, which were similar to each other. These results point out the importance of 1) examining other data sets to examine long-term impact of assisted reproductive technologies on adult physiology and performance and 2) evaluating whether use of sexed semen alters the adult phenotype when used for artificial insemination
Keywords
References
Agung B, Otoi T, Wongsrikeao P, Taniguchi M, Shimizu R, Watari H, Nagai T. 2006. Effect of maturation culture period of oocytes on the sex ratio of in vitro fertilized bovine embryos. J Reprod Dev, 52:123-127.
Block J, Bonilla L, Hansen PJ. 2010. Efficacy of in vitro embryo transfer in lactating dairy cows using fresh or vitrified embryos produced in a novel embryo culture medium. J Dairy Sci, 93:5234-2542.
Bonilla L, Block J, Denicol AC, Hansen PJ. 2014. Consequences of transfer of an in vitro-produced embryo for the dam and resultant calf. J Dairy Sci,97:229-239.
Calle A, Miranda A, Fernandez-Gonzalez R, Pericuesta E, Laguna R, Gutierrez-Adan A. 2012. Male mice produced by in vitro culture have reduced fertility and transmit organomegaly and glucose intolerance to their male offspring. Biol Reprod, 87:34. doi: 10.1095/biolreprod.112.100743.
Canu S, Boland M, Lloyd GM, Newman M, Christie MF, May PJ, Christley RM, Smith RF, Dobson H. 2010. Predisposition to repeat breeding in UK cattle and success of artificial insemination alone or in combination with embryo transfer. Vet Rec, 167:44-51.
Ceelen M, van Weissenbruch MM, Roos JC, Vermeiden JP, van Leeuwen FE, Delemarre-van de Waal HA. 2007. Body composition in children and adolescents born after in vitro fertilization or spontaneous conception. J Clin Endocrinol Metab, 92:3417-3423.
Cerny D, Sartori C, Rimoldi SF, Meister T, Soria R, Bouillet E, Scherrer U, Rexhaj E. 2017. Assisted reproductive technologies predispose to insulin resistance and obesity in male mice challenged with a high fat diet. Endocrinology, 158:1152-1159.
DeJarnette JM, Nebel RL, Marshall CE. 2009. Evaluating the success of sex-sorted semen in US dairy herds from on farm records. Theriogenology, 71:49-58.
Donjacour A, Liu X, Lin W, Simbulan R, Rinaudo PF. 2014. In vitro fertilization affects growth and glucose metabolism in a sex-specific manner in an outbred mouse model. Biol Reprod, 90:80. doi: 10.1095/biolreprod.113.113134.
Ecker DJ, Stein P, Xu Z, Williams CJ, Kopf GS, Bilker WB, Abel T, Schultz RM. 2004. Long-term effects of culture of preimplantation mouse embryos on behavior. Proc Natl Acad Sci USA, 101:1595-600.
Farin CE, Farmer WT, Farin PW. 2010. Pregnancy recognition and abnormal offspring syndrome in cattle. Reprod Fertil Dev, 22:75-87.
Fernández-Gonzalez R, Moreira P, Bilbao A, Jiménez A, Pérez-Crespo M, Ramírez MA, Rodríguez De Fonseca F, Pintado B, Gutiérrez-Adán A. 2004. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc Natl Acad Sci USA, 101:5880-5885.
Fleming TP, Watkins AJ, Sun C, Velazquez MA, Smyth NR, Eckert JJ. 2015. Do little embryos make big decisions? How maternal dietary protein restriction can permanently change an embryo's potential, affecting adult health. Reprod Fertil Dev, 27:684-692.
Gad A, Besenfelder U, Rings F, Ghanem N, SalilewWondim D, Hossain MM, Tesfaye D, Lonergan P, Becker A, Cinar U, Schellander K, Havlicek V, Hölker M. 2011. Effect of reproductive tract environment following controlled ovarian hyperstimulation treatment on embryo development and global transcriptome profile of blastocysts: implications for animal breeding and human assisted reproduction.
Hum Reprod, 26:1693-707. Hansen PJ. 2006. Realizing the promise of IVF in cattle--an overview. Theriogenology, 65:119-125.
Hansen PJ. 2014. Current and future assisted reproductive technologies for mammalian farm animals. Adv Exp Med Biol, 752:1-22.
Hansen, PJ. 2015. Developmental programming in the preimplantation period: can it be exploited to enhance postnatal function in cattle? Anim Reprod, 12:428-436. Hansen PJ, Dobbs KB, Denicol AC, Siqueira LG.
2016. Sex and the preimplantation embryo: implications of sexual dimorphism in the preimplantation period for maternal programming of embryonic development. Cell Tissue Res, 363:237-247.
Healy AA, House JK, Thomson PC. 2013. Artificial insemination field data on the use of sexed and conventional semen in nulliparous Holstein heifers. J Dairy Sci, 96:1905-1914.
Hinde K, Carpenter AJ, Clay JS, Bradford BJ. 2014. Holsteins favor heifers, not bulls: biased milk production programmed during pregnancy as a function of fetal sex. PLoS One, 9:e86169.
Kaniyamattam K, Block J, Hansen PJ, De Vries A. 2017. Comparison between an exclusive in vitroproduced embryo transfer system and artificial insemination for genetic, technical, and financial herd performance. J Dairy Sci, 100: 5729-5745.
Koyama K, Kang SS, Huang W, Yanagawa Y, Takahashi Y, Nagano M. 2014. Aging-related changes in in vitro-matured bovine oocytes: oxidative stress, mitochondrial activity and ATP content after nuclear maturation. J Reprod Dev, 60:136-142.
Liu W-M, Pang RTK, Chiu PCN, Wong BPC, Lao K, Lao, KF, Yeung WSB. 2012. Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc Natl Acad Sci USA, 109:490- 494.
Mahsoudi B, Li A, O'Neill C. 2007. Assessment of the long-term and transgenerational consequences of perturbing preimplantation embryo development in mice. Biol Reprod, 77:889-896.
Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Mann MRW. 2010. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum Mol Genet, 19:36-51.
Pellegrino CA, Morotti F, Untura RM, Pontes JH, Pellegrino MF, Campolina JP, Seneda MM, Barbosa FA, Henry M. 2016. Use of sexed sorted semen for fixed-time artificial insemination or fixed-time embryo transfer of in vitro-produced embryos in cattle. Theriogenology, 86:888-893.
Pereira MH, Wiltbank MC, Vasconcelos JL. 2016. Expression of estrus improves fertility and decreases pregnancy losses in lactating dairy cows that receive artificial insemination or embryo transfer. J Dairy Sci, 99:2237-2247.
Pontes JH, Nonato-Junior I, Sanches BV, ErenoJunior JC, Uvo S, Barreiros TR, Oliveira JA, Hasler JF, Seneda MM. 2009. Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows. Theriogenology, 71:690-697.
Pontes JH, Silva KC, Basso AC, Rigo AG, Ferreira CR, Santos GM, Sanches BV, Porcionato JP, Vieira PH, Faifer FS, Sterza FA, Schenk 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.
Pryce JE, Goddard ME, Raadsma HW, Hayes BJ. 2010. Deterministic models of breeding scheme designs that incorporate genomic selection. J Dairy Sci, 93:5455-5466
Rando OJ, Simmons RA. 2015. I’m eating for two: parental dietary effects on offspring metabolism. Cell, 161:93-105.
Rasmussen S, Block J, Seidel GE Jr, Brink Z, McSweeney K, Farin PW, Bonilla L, Hansen PJ. 2013. Pregnancy rates of lactating cows after transfer of in vitro produced embryos using X-sorted sperm. Theriogenology. 79:453-461.
Rexhaj E, Pireva A, Paoloni-Giacobino A, Allemann Y, Cerny D, Dessen P, Sartori C, Scherrer U, Rimoldi SF. 2015. Prevention of vascular dysfunction and arterial hypertension in mice generated by assisted reproductive technologies by addition of melatonin to culture media. Am J Physiol Heart Circ Physiol, 309:H1151-1156.
Schagdarsurengin U, Steger K. 2016. Epigenetics in male reproduction: effect of paternal diet on sperm quality and offspring health. Nat Rev Urol, 13:584-595.
Scherrer U, Rexhaj E, Allemann Y, Sartori C, Rimoldi SF. 2015. Cardiovascular dysfunction in children conceived by assisted reproductive technologies. Eur Heart J, 36:1583-1589.
Siqueira LG, Torres CA, Souza ED, Monteiro PL Jr, Arashiro EK, Camargo LS, Fernandes CA, Viana JH. 2009. Pregnancy rates and corpus luteum-related factors affecting pregnancy establishment in bovine recipients synchronized for fixed-time embryo transfer. Theriogenology, 72:949-958.
Siqueira LGB, Dikmen S, Ortega MS, Hansen PJ. 2017a. Postnatal phenotype of dairy cows is altered by in vitro embryo production using reverse X-sorted semen. J Dairy Sci, 100:5899-5908.
Siqueira, LGB, Tribulo P, Chen Z, Denicol AC, Ortega MS,Negrón-Pérez WM, KannampuzhaFrancis J, Pohler KG, Rivera RM, Hansen PJ. 2017b. Colony stimulating factor 2 acts from Days 5 to 7 of development to modify programming of the bovine conceptus at day 86 of gestation. Biol Reprod, 96:743-757.
Son DS, Choe CY, Cho SR, Choi SH, Kim HJ, Hur TY, Jung YG, Kang HG, Kim IM. 2007. A CIDRbased timed embryo transfer protocol increases the pregnancy rate of lactating repeat breeder dairy cows. J Reprod Dev, 53:1313-1318.
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.
Strata F, Giritharan G, Sebastiano FD, Piane LD, Kao CN, Donjacour A, Rinaudo P. 2015. Behavior and brain gene expression changes in mice exposed to preimplantation and prenatal stress. Reprod Sci, 22:23- 30.
Thomasen JR, Willam A, Egger-Danner C, Sørensen AC. 2016. Reproductive technologies combine well with genomic selection in dairy breeding programs. J Dairy Sci, 99:1331-1340.
Turner N, Robker RL. 2015. Developmental programming of obesity and insulin resistance: does mitochondrial dysfunction in oocytes play a role? Mol Hum Reprod, 21:23-30.
van Wagtendonk-de Leeuw AM, Aerts BJ, den Daas JH. 1998. Abnormal offspring following in vitro production of bovine preimplantation embryos: a field study. Theriogenology, 49:883-894.
Vasconcelos JL, Jardina DT, Sá Filho OG, Aragon FL, Veras MB. 2011. Comparison of progesteronebased protocols with gonadotropin-releasing hormone or estradiol benzoate for timed artificial insemination or embryo transfer in lactating dairy cows. Theriogenology, 75:1153-1160.
Wagenaar K, Ceelen M, van Weissenbruch MM, Knol DL, Delemarre-van de Waal HA, Huisman J. 2008. School functioning in 8- to 18-year-old children born after in vitro fertilization. Eur J Pediatr, 167:1289- 1295.
Watkins AJ, Platt D, Papenbrock T, Wilkins A, Eckert JJ, Kwong WY, Osmond C, Hanson M, Fleming TP. 2007. Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure. Proc Natl Acad Sci USA, 104:5449- 5454.
Watkins AJ, Wilkins A, Cunningham C, Perry VH, Seet MJ, Osmond C, Eckert JJ, Torrens C, Cagampang FR, Cleal J, Gray WP, Hanson MA, Fleming TP. 2008. Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol, 586:2231-2244.
Wheeler MB, Rutledge JJ, Fischer-Brown A, VanEtten T, Malusky S, Beebe DJ. 2006. Application of sexed semen technology to in vitro embryo production in cattle. Theriogenology, 65:219-227.
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email