Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
REVIEW

In vitro manipulation techniques of porcine embryos: a meta-analysis related to transfers, pregnancies and piglets

Ying Liu A E , Juan Li A B , Peter Løvendahl C , Mette Schmidt D , Knud Larsen C and Henrik Callesen A

A Reproductive Biology, Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.

B College of Animal Science and Technology, Nanjing Agricultural University, 210095 Jiangsu Province, Nanjing Wei Gang No. 1, China.

C Department of Molecular Biology and Genetics, Aarhus University, DK-8830 Tjele, Denmark.

D Department of Large Animal Sciences, Faculty of Life Science, University of Copenhagen, DK-1870 Frederiksberg C, Denmark.

E Corresponding author. Email: ying.liu@agrsci.dk

Reproduction, Fertility and Development 27(3) 429-439 https://doi.org/10.1071/RD13329
Submitted: 26 September 2013  Accepted: 21 January 2014   Published: 24 February 2014

Abstract

During the last 17 years, considerable advancements have been achieved in the production of pigs, transgenic and non-transgenic, by methods of somatic cell nuclear transfer, in vitro fertilisation, intracytoplasmic sperm injection, microinjection and sperm-mediated gene transfer by artificial insemination. Therefore, a review of the overall efficiency for the developmental competence of embryos produced by these in vitro methods would be useful in order to obtain a more thorough overview of this growing area with respect to its development and present status. In this review a meta-analysis was used to analyse data collected from all published articles with a focus on zygotes and embryos for transfer, pregnancy, full-term development and piglets born. It was generally concluded that an increasing level of in vitro manipulation of porcine embryos decreased the overall efficiency for production of piglets. The techniques of nuclear transfer have been developed markedly through the increasing number of studies performed, and the results have become more stable. Prolonged in vitro culture period did not lead to any negative effect on nuclear transfer embryos after their transfer and it resulted in a similar or even higher litter size. More complete information is needed in future scientific articles about these in vitro manipulation techniques to establish a more solid basis for the evaluation of their status and to reveal and further investigate any eventual problems.

Additional keywords: nuclear transfer, pig, transgenic.


References

Abeydeera, L. R., Johnson, L. A., Welch, G. R., Wang, W. H., Boquest, A. C., Cantley, T. C., Rieke, A., and Day, B. N. (1998). Birth of piglets preselected for gender following in vitro fertilisation of in vitro-matured pig oocytes by X and Y chromosome-bearing spermatozoa sorted by high-speed flow cytometry. Theriogenology 50, 981–988.
Birth of piglets preselected for gender following in vitro fertilisation of in vitro-matured pig oocytes by X and Y chromosome-bearing spermatozoa sorted by high-speed flow cytometry.CrossRef | 1:STN:280:DC%2BD3c7pvVGqsA%3D%3D&md5=68580458bbdb18b8d682078eb246578dCAS | 10734417PubMed | open url image1

Al-Mashhadi, R. H., Sorensen, C. B., Kragh, P. M., Christoffersen, C., Mortensen, M. B., Tolbod, L. P., Thim, T., Du, Y. T., Li, J., Liu, Y., Moldt, B., Schmidt, M., Vajta, G., Larsen, T., Purup, S., Bolund, L., Nielsen, L. B., Callesen, H., Falk, E., Mikkelsen, J. G., and Bentzon, J. F. (2013). Familial hypercholesterolemia and atherosclerosis in cloned minipigs created by DNA transposition of a human PCSK9 gain-of-function mutant. Sci. Transl. Med. 5, 166ra1.
Familial hypercholesterolemia and atherosclerosis in cloned minipigs created by DNA transposition of a human PCSK9 gain-of-function mutant.CrossRef | 23283366PubMed | open url image1

Besenfelder, U., Modl, J., Muller, M., and Brem, G. (1997). Endoscopic embryo collection and embryo transfer into the oviduct and the uterus of pigs. Theriogenology 47, 1051–1060.
Endoscopic embryo collection and embryo transfer into the oviduct and the uterus of pigs.CrossRef | 1:STN:280:DC%2BD28zgtVyjtQ%3D%3D&md5=7c784a199d9d51cf90e5e014c9d66eaeCAS | 16728055PubMed | open url image1

Bryla, M., Trzcinska, M., and Wieczorek, J. (2009). Analysis of in vivo- and in vitro-derived pig expanded blastocysts based on DNA fragmentation. Anim. Sci. Pap. Rep. 27, 59–68. open url image1

Chavatte-Palmer, P., Lee, R., Bertolini, M., Jammes, H., Schmidt, M., and Callesen, H. (2013). Pregnancy and neonatal care of SCNT animals. In ‘Principles of Cloning’. 2nd edn. (Eds J. Cibelli, J. Gurdon, I. Wilmut, R. Jaenisch, R. Lanza, M. D. West, K. H. S. Campbell.) pp. 107–126. (Elsevier Inc.: Amsterdam, the Netherlands.)

Deshmukh, R. S., Ostrup, O., Ostrup, E., Vejlsted, M., Niemann, H., Lucas-Hahn, A., Petersen, B., Li, J. A., Callesen, H., and Hyttel, P. (2011). DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilisation, parthenogenetic activation and somatic cell nuclear transfer. Epigenetics 6, 177–187.
DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilisation, parthenogenetic activation and somatic cell nuclear transfer.CrossRef | 1:CAS:528:DC%2BC3MXjs12ksLY%3D&md5=591615abb4092ec0f1627d508d4fabb7CAS | 20935454PubMed | open url image1

Farin, P. W., Piedrahita, J. A., and Farin, C. E. (2006). Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology 65, 178–191.
Errors in development of fetuses and placentas from in vitro-produced bovine embryos.CrossRef | 16266745PubMed | open url image1

Farin, C. E., Farmer, W. T., and Farin, P. W. (2010). Pregnancy recognition and abnormal offspring syndrome in cattle. Reprod. Fertil. Dev. 22, 75–87.
Pregnancy recognition and abnormal offspring syndrome in cattle.CrossRef | 1:CAS:528:DC%2BC3cXitlagurc%3D&md5=284a97db4fd582185a4e789cdce14867CAS | 20003848PubMed | open url image1

García-Roselló, E., García-Mengual, E., Coy, P., Alfonso, J., and Silvestre, M. A. (2009). Intracytoplasmic sperm injection in livestock species: an update. Reprod. Domest. Anim. 44, 143–151.
Intracytoplasmic sperm injection in livestock species: an update.CrossRef | 18954388PubMed | open url image1

Isom, S. C., Stevens, J. R., Li, R. F., Spollen, W. G., Cox, L., Spate, L. D., Murphy, C. N., and Prather, R. S. (2013). Transcriptional profiling by RNA-Seq of peri-attachment porcine embryos generated by a variety of assisted reproductive technologies. Physiol. Genomics 45, 577–589.
Transcriptional profiling by RNA-Seq of peri-attachment porcine embryos generated by a variety of assisted reproductive technologies.CrossRef | 1:CAS:528:DC%2BC3sXht1OmtLjE&md5=75b213fa6e61a4ac95beb952592629a6CAS | 23695885PubMed | open url image1

Jakobsen, J. E., Li, J., Kragh, P. M., Moldt, B., Lin, L., Liu, Y., Schmidt, M., Winther, K. D., Schyth, B. D., Holm, I. E., Vajta, G., Bolund, L., Callesen, H., Jorgensen, A. L., Nielsen, A. L., and Mikkelsen, J. G. (2011). Pig transgenesis by Sleeping Beauty DNA transposition. Transgenic Res. 20, 533–545.
Pig transgenesis by Sleeping Beauty DNA transposition.CrossRef | 1:CAS:528:DC%2BC3MXlslKhsbc%3D&md5=dc9de636e8844fa24117a3cd5a5cc731CAS | 20803249PubMed | open url image1

Kikuchi, K., Kashiwazaki, N., Noguchi, J., Shimada, A., Takahashi, R., Hirabayashi, M., Shino, M., Ueda, M., and Kaneko, H. (1999). Developmental competence, after transfer to recipients, of porcine oocytes matured, fertilised and cultured in vitro. Biol. Reprod. 60, 336–340.
Developmental competence, after transfer to recipients, of porcine oocytes matured, fertilised and cultured in vitro.CrossRef | 1:CAS:528:DyaK1MXotlyhtQ%3D%3D&md5=47a02071ba9fc27027c44340af7e42bfCAS | 9915999PubMed | open url image1

Kolbe, T., and Holtz, W. (2000). Birth of a piglet derived from an oocyte fertilised by intracytoplasmic sperm injection (ICSI). Anim. Reprod. Sci. 64, 97–101.
Birth of a piglet derived from an oocyte fertilised by intracytoplasmic sperm injection (ICSI).CrossRef | 1:STN:280:DC%2BD3M%2FmslWktA%3D%3D&md5=776ea70ced6912a11197ae0dfa3424b8CAS | 11078970PubMed | open url image1

Kragh, P. M., Nielsen, A. L., Li, J., Du, Y. T., Lin, L., Schmidt, M., Bogh, I. B., Holm, I. E., Jakobsen, J. E., Johansen, M. G., Purup, S., Bolund, L., Vajta, G., and Jorgensen, A. L. (2009). Hemizygous minipigs produced by random gene insertion and handmade cloning express the Alzheimer’s disease-causing dominant mutation APPsw. Transgenic Res. 18, 545–558.
Hemizygous minipigs produced by random gene insertion and handmade cloning express the Alzheimer’s disease-causing dominant mutation APPsw.CrossRef | 1:CAS:528:DC%2BD1MXnvFKisLs%3D&md5=4d5f85fe9296ed1e19a383b0899b0704CAS | 19184503PubMed | open url image1

Kruip, T. A. M., and den Daas, J. H. G. (1997). In vitro-produced and cloned embryos: effects on pregnancy, parturition and offspring. Theriogenology 47, 43–52.
In vitro-produced and cloned embryos: effects on pregnancy, parturition and offspring.CrossRef | open url image1

Kurome, M., Geistlinger, L., Kessler, B., Zakhartchenko, V., Klymiuk, N., Wuensch, A., Richter, A., Baehr, A., Kraehe, K., Burkhardt, K., Flisikowski, K., Flisikowska, T., Merkl, C., Landmann, M., Durkovic, M., Tschukes, A., Kraner, S., Schindelhauer, D., Petri, T., Kind, A., Nagashima, H., Schnieke, A., Zimmer, R., and Wolf, E. (2013). Factors influencing the efficiency of generating genetically engineered pigs by nuclear transfer: multi-factorial analysis of a large data set. BMC Biotechnol. 13, 43.
Factors influencing the efficiency of generating genetically engineered pigs by nuclear transfer: multi-factorial analysis of a large data set.CrossRef | 1:CAS:528:DC%2BC3sXhtFKktLrE&md5=fc435cc034e85098ca3ec239a2b06490CAS | 23688045PubMed | open url image1

Lai, L. X., Kang, J. X., Li, R. F., Wang, J. D., Witt, W. T., Yong, H. Y., Hao, Y. H., Wax, D. M., Murphy, C. N., Rieke, A., Samuel, M., Linville, M. L., Korte, S. W., Evans, R. W., Starzl, T. E., Prather, R. S., and Dai, Y. F. (2006). Generation of cloned transgenic pigs rich in omega-3 fatty acids. Nat. Biotechnol. 24, 435–436.
Generation of cloned transgenic pigs rich in omega-3 fatty acids.CrossRef | 1:CAS:528:DC%2BD28Xjt1Wisb4%3D&md5=0ed7f01e0027fd57446c8bf68b9a1391CAS | open url image1

Lavitrano, M., Forni, M., Varzi, V., Pucci, L., Bacci, M. L., Di Stefano, C., Fioretti, D., Zoraqi, G., Moioli, B., Rossi, M., Lazzereschi, D., Stoppacciaro, A., Seren, E., Alfani, D., Cortesini, R., and Frati, L. (1997). Sperm-mediated gene transfer: production of pigs transgenic for a human regulator of complement activation. Transplant. Proc. 29, 3508–3509.
Sperm-mediated gene transfer: production of pigs transgenic for a human regulator of complement activation.CrossRef | 1:CAS:528:DyaK1cXht1aktg%3D%3D&md5=eced5e87d1f7a77dd27d2825c9ebc184CAS | 9414813PubMed | open url image1

Lee, K., Redel, B. K., Spate, L., Teson, J., Brown, A. N., Park, K. W., Walters, E., Samuel, M., Murphy, C. N., and Prather, R. S. (2013). Piglets produced from cloned blastocysts cultured in vitro with GM-CSF. Mol. Reprod. Dev. 80, 145–154.
Piglets produced from cloned blastocysts cultured in vitro with GM-CSF.CrossRef | 1:CAS:528:DC%2BC3sXhtFOis7w%3D&md5=914068d8da8c4205ed9bb07e89d55c8cCAS | 23239239PubMed | open url image1

Luo, Y. L., Li, J., Liu, Y., Lin, L., Du, Y. T., Li, S. T., Yang, H. M., Vajta, G., Callesen, H., Bolund, L., and Sorensen, C. B. (2011). High efficiency of BRCA1 knockout using rAAV-mediated gene targeting: developing a pig model for breast cancer. Transgenic Res. 20, 975–988.
High efficiency of BRCA1 knockout using rAAV-mediated gene targeting: developing a pig model for breast cancer.CrossRef | 1:CAS:528:DC%2BC3MXhtFKrt7%2FL&md5=1c3fe6319836c2a5c4d8620e8578442aCAS | open url image1

Mulley, R. C., and Edwards, M. J. (1984). Prevalence of congenital abnormalities in pigs. Aust. Vet. J. 61, 116–120.
Prevalence of congenital abnormalities in pigs.CrossRef | 1:STN:280:DyaL2c3ls1enuw%3D%3D&md5=ba4c9375a3ef1ae463e285562c415206CAS | 6540081PubMed | open url image1

Nagashima, H., Fujimura, T., Takahagi, Y., Kurome, M., Wako, N., Ochiai, T., Esaki, R., Kano, K., Saito, S., Okabe, M., and Murakami, H. (2003). Development of efficient strategies for the production of genetically modified pigs. Theriogenology 59, 95–106.
Development of efficient strategies for the production of genetically modified pigs.CrossRef | 1:CAS:528:DC%2BD38XpslSmurY%3D&md5=5e075f31e748f1ae94090557c2ab2ec2CAS | 12499021PubMed | open url image1

Niemann, H., Kues, W. A., Lucas-Hahn, A., and Carnwath, J. W. (2010). Somatic cloning and epigenetic reprogramming in mammals. In ‘Principles of Regenerative Medicine’. 2nd edn. (Eds A. Atala, R. Lanza, J. A. Thomson, R. Nerem.) pp. 129–158. (Elsevier Inc.: Amsterdam, the Netherlands.)

Partlow, G. D., Fisher, K. R. S., Page, P. D., Macmillan, K., and Walker, A. F. (1993). Prevalence and types of birth defects in Ontario swine determined by mail survey. Can. J. Vet. Res. 57, 67–73.
| 1:STN:280:DyaK3s3lvVKitw%3D%3D&md5=aa56f8d198f7b43d6cb9eac31f453e5dCAS | 8490809PubMed | open url image1

Polejaeva, I. A., Chen, S. H., Vaught, T. D., Page, R. L., Mullins, J., Ball, S., Dai, Y. F., Boone, J., Walker, S., Ayares, D. L., Colman, A., and Campbell, K. H. S. (2000). Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407, 86–90.
Cloned pigs produced by nuclear transfer from adult somatic cells.CrossRef | 1:STN:280:DC%2BD3cvkt12rug%3D%3D&md5=7fac45af8aa3c71cf21c56e16986794eCAS | 10993078PubMed | open url image1

Pomar, F. J. R., Teerds, K. J., Kidson, A., Colenbrander, B., Tharasanit, T., Aguilar, B., and Roelen, B. A. J. (2005). Differences in the incidence of apoptosis between in vivo- and in vitro-produced blastocysts of farm animal species: a comparative study. Theriogenology 63, 2254–2268.
Differences in the incidence of apoptosis between in vivo- and in vitro-produced blastocysts of farm animal species: a comparative study.CrossRef | 1:CAS:528:DC%2BD2MXjtFyrtbg%3D&md5=a25eb98906651be6f0b970fcda5bf9ecCAS | open url image1

Schmidt, M., Winter, K. D., Dantzer, V., Li, J., Kragh, P. M., Du, Y., Lin, L., Liu, Y., Vajta, G., Sangild, P. T., Callesen, H., and Agerholm, J. S. (2011). Maternal endometrial oedema may increase perinatal mortality of cloned and transgenic piglets. Reprod. Fertil. Dev. 23, 645–653.
Maternal endometrial oedema may increase perinatal mortality of cloned and transgenic piglets.CrossRef | 1:STN:280:DC%2BC3MrntFeruw%3D%3D&md5=ef40c9c1c5e718e32c62e307df8608e3CAS | 21635813PubMed | open url image1

Uchida, M., Shimatsu, Y., Onoe, K., Matsuyama, N., Niki, R., Ikeda, J. E., and Imai, H. (2001). Production of transgenic miniature pigs by pronuclear microinjection. Transgenic Res. 10, 577–582.
Production of transgenic miniature pigs by pronuclear microinjection.CrossRef | 1:CAS:528:DC%2BD38XmtlSksQ%3D%3D&md5=0b5b938e6d901b361d31b481cf0e2df2CAS | 11817545PubMed | open url image1

Vajta, G., Zhang, Y. H., and Machaty, Z. (2007). Somatic cell nuclear transfer in pigs: recent achievements and future possibilities. Reprod. Fertil. Dev. 19, 403–423.
Somatic cell nuclear transfer in pigs: recent achievements and future possibilities.CrossRef | 17257528PubMed | open url image1

Vazquez, J. M., Martinez, E. A., Parrilla, I., Roca, J., Gil, M. A., and Vazquez, J. L. (2003). Birth of piglets after deep intrauterine insemination with flow cytometrically sorted boar spermatozoa. Theriogenology 59, 1605–1614.
Birth of piglets after deep intrauterine insemination with flow cytometrically sorted boar spermatozoa.CrossRef | 12559465PubMed | open url image1



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