Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effects of antifreeze glycoprotein 8 (AFGP8) supplementation during vitrification on the in vitro developmental capacity of expanded bovine blastocysts

Shuang Liang A * , Bao Yuan A B * , Yong-Xun Jin B C * , Jia-Bao Zhang B , Jeong Kyu Bang D and Nam-Hyung Kim A B E
+ Author Affiliations
- Author Affiliations

A Department of Animal Science, Chungbuk National University, Naesudong-ro, Seowon-gu, Cheongju-si, Chungcheongbuk-do, 28864, Republic of Korea.

B Department of Laboratory Animal Center, College of Animal Sciences, Jilin University, Xi’an Road 5333, Changchun, Jilin, 130062, China.

C Sooam Biotech Research Foundation, 64 Kyunginro, Guro-gu, Seoul, 152-895, Republic of Korea.

D Division of Magnetic Resonance, Korea Basic Science Institute, Ochang, Chung-Buk, 363-883, Republic of Korea.

E Corresponding author. Email: nhkim@chungbuk.ac.kr

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16426
Submitted: 5 August 2016  Accepted: 19 January 2017   Published online: 28 February 2017

Abstract

Cryopreservation is an effective method for the long-term storage of valuable germplasm in the field of reproductive research. The present study examined the developmental capacity of post-thaw bovine blastocysts during vitrification after supplementation with antifreeze glycoprotein 8 (AFGP8). Survival and re-expansion rates in culture during the 12 h after thawing were significantly higher in the AFGP8-treated than untreated group. In addition, blastocysts from the AFGP8-treated group exhibited lower rates of apoptosis. Real-time reverse transcription–polymerase chain reaction analysis showed that the expression of the Bcl-2 gene, coding for an anti-apoptotic protein, was increased significantly, whereas the expression of the pro-apoptotic gene Bax was decreased significantly in the AFGP8-treated group. The cellular proliferation rate and mitochondrial membrane potential were significantly higher in post-thaw re-expanded blastocysts from the AFGP8-treated compared with untreated group. In addition, outgrowth potential in post-thaw blastocysts in re-expanded blastocysts after vitrification was significantly increased in the AFGP8-treated compared with untreated group. Together, these results are the first to demonstrate that the addition of AFGP8 during vitrification can help protect bovine blastocysts against chill-induced injury.

Additional keywords: embryos, cryopreservation.


References

Acton, B. M., Jurisicova, A., Jurisica, I., and Casper, R. F. (2004). Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol. Hum. Reprod. 10, 23–32.
Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development.CrossRef | 1:CAS:528:DC%2BD3sXpvVeltro%3D&md5=c789add60f77307112c300f1fd6af59fCAS | open url image1

Ahn, M., Murugan, R. N., Shin, S. Y., Kim, H. J., and Bang, J. K. (2012). Peptoid-based positional scanning derivatives: revealing the optimum residue required for ice recrystallization inhibition activity for every position in the AFGPs. Bull. Korean Chem. Soc. 33, 3931–3932.
Peptoid-based positional scanning derivatives: revealing the optimum residue required for ice recrystallization inhibition activity for every position in the AFGPs.CrossRef | 1:CAS:528:DC%2BC3sXlvFSrtw%3D%3D&md5=011ad82a7521a75003ed2427210c4948CAS | open url image1

Bang, J. K., Lee, J. H., Murugan, R. N., Lee, S. G., Do, H., Koh, H. Y., Shim, H.-E., Kim, H.-C., and Kim, H. J. (2013). Antifreeze peptides and glycopeptides, and their derivatives: potential uses in biotechnology. Mar. Drugs 11, 2013–2041.
Antifreeze peptides and glycopeptides, and their derivatives: potential uses in biotechnology.CrossRef | open url image1

Choi, J., Park, S. M., Lee, E., Kim, J. H., Jeong, Y. I., Lee, J. Y., Park, S. W., Kim, H. S., Hossein, M. S., and Jeong, Y. W. (2008). Anti-apoptotic effect of melatonin on preimplantation development of porcine parthenogenetic embryos. Mol. Reprod. Dev. 75, 1127–1135.
Anti-apoptotic effect of melatonin on preimplantation development of porcine parthenogenetic embryos.CrossRef | 1:CAS:528:DC%2BD1cXntFWgt7w%3D&md5=777a6ac1cb95cfd75f63fb0d76df8e16CAS | open url image1

Dai, J., Wu, C., Muneri, C. W., Niu, Y., Zhang, S., Rui, R., and Zhang, D. (2015). Changes in mitochondrial function in porcine vitrified MII-stage oocytes and their impacts on apoptosis and developmental ability. Cryobiology 71, 291–298.
Changes in mitochondrial function in porcine vitrified MII-stage oocytes and their impacts on apoptosis and developmental ability.CrossRef | 1:CAS:528:DC%2BC2MXht1ygs7rP&md5=e7a1518a548c41e3ce1cb648efdb6d69CAS | open url image1

Dumollard, R., Duchen, M., and Carroll, J. (2007). The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77, 21–49.
The role of mitochondrial function in the oocyte and embryo.CrossRef | 1:CAS:528:DC%2BD2sXmt1Gltb4%3D&md5=95aed99d5fcb130a72ea5b434e1b1d39CAS | open url image1

Exley, G. E., Tang, C., McElhinny, A. S., and Warner, C. M. (1999). Expression of caspase and BCL-2 apoptotic family members in mouse preimplantation embryos. Biol. Reprod. 61, 231–239.
Expression of caspase and BCL-2 apoptotic family members in mouse preimplantation embryos.CrossRef | 1:CAS:528:DyaK1MXktFKgu7g%3D&md5=6a38da8495fee1b19c996c6ba8c21c35CAS | open url image1

Findikli, N., Kahraman, S., Kumtepe, Y., Donmez, E., Benkhalifa, M., Biricik, A., Sertyel, S., Berkil, H., and Oncu, N. (2004). Assessment of DNA fragmentation and aneuploidy on poor quality human embryos. Reprod. Biomed. Online 8, 196–206.
Assessment of DNA fragmentation and aneuploidy on poor quality human embryos.CrossRef | 1:CAS:528:DC%2BD2cXitVeisbw%3D&md5=ae96382d45193866f13aea35de30e79dCAS | open url image1

Ha, A.-N., Lee, S.-R., Jeon, J.-S., Park, H.-S., Lee, S.-H., Jin, J.-I., Sessions, B. R., Wang, Z., White, K. L., and Kong, I.-K. (2014). Development of a modified straw method for vitrification of in vitro-produced bovine blastocysts and various genes expression in between the methods. Cryobiology 68, 57–64.
Development of a modified straw method for vitrification of in vitro-produced bovine blastocysts and various genes expression in between the methods.CrossRef | 1:CAS:528:DC%2BC3sXhvFyqsL%2FF&md5=585957dc1e19077e1bccdd218d0715a2CAS | open url image1

Hosseini, S. M., Forouzanfar, M., Hajian, M., Asgari, V., Abedi, P., Hosseini, L., Ostadhosseini, S., Moulavi, F., Langrroodi, M. S., Sadeghi, H., Bahramian, H., Eghbalsaied, S., and Nasr-Esfahani, M. H. (2009). Antioxidant supplementation of culture medium during embryo development and/or after vitrification-warming; which is the most important? J. Assist. Reprod. Genet. 26, 355–364.
Antioxidant supplementation of culture medium during embryo development and/or after vitrification-warming; which is the most important?CrossRef | 1:STN:280:DC%2BD1MrmslCgtw%3D%3D&md5=4194a8ce4c8677e19a84ac6ca6dbec10CAS | open url image1

Inaba, Y., Miyashita, S., Somfai, T., Geshi, M., Matoba, S., Dochi, O., and Nagai, T. (2016). Cryopreservation method affects DNA fragmentation in trophectoderm and the speed of re-expansion in bovine blastocysts. Cryobiology 72, 86–92.
Cryopreservation method affects DNA fragmentation in trophectoderm and the speed of re-expansion in bovine blastocysts.CrossRef | 1:CAS:528:DC%2BC28Xksl2lsrk%3D&md5=74b147782e4ee9ae202f2a1f64769de1CAS | open url image1

Jakobsen, A. S., Thomsen, P. D., and Avery, B. (2006). Few polyploid blastomeres in morphologically superior bovine embryos produced in vitro. Theriogenology 65, 870–881.
Few polyploid blastomeres in morphologically superior bovine embryos produced in vitro.CrossRef | open url image1

Jia, Z., and Davies, P. L. (2002). Antifreeze proteins: an unusual receptor–ligand interaction. Trends Biochem. Sci. 27, 101–106.
Antifreeze proteins: an unusual receptor–ligand interaction.CrossRef | 1:CAS:528:DC%2BD38XhtlGjur4%3D&md5=413397a714b7f64e006c10d360c5ee5dCAS | open url image1

Jiang, Z., Harrington, P., Zhang, M., Marjani, S. L., Park, J., Kuo, L., Pribenszky, C., and Tian, X. C. (2016). Effects of high hydrostatic pressure on expression profiles of in vitro produced vitrified bovine blastocysts. Sci. Rep. 6, 21215.
Effects of high hydrostatic pressure on expression profiles of in vitro produced vitrified bovine blastocysts.CrossRef | 1:CAS:528:DC%2BC28Xislynsb4%3D&md5=217a4975271da65a9ec69373069f59e2CAS | open url image1

Jo, J. W., Jee, B. C., Suh, C. S., and Kim, S. H. (2012). The beneficial effects of antifreeze proteins in the vitrification of immature mouse oocytes. PLoS One 7, e37043.
The beneficial effects of antifreeze proteins in the vitrification of immature mouse oocytes.CrossRef | 1:CAS:528:DC%2BC38XotVyru7s%3D&md5=65e82b869921cb86812149e77a4939e6CAS | open url image1

Knijn, H. M., Gjørret, J. O., Vos, P. L., Hendriksen, P. J., van der Weijden, B. C., Maddox-Hyttel, P., and Dieleman, S. J. (2003). Consequences of in vivo development and subsequent culture on apoptosis, cell number, and blastocyst formation in bovine embryos. Biol. Reprod. 69, 1371–1378.
Consequences of in vivo development and subsequent culture on apoptosis, cell number, and blastocyst formation in bovine embryos.CrossRef | 1:CAS:528:DC%2BD3sXnsV2nsbs%3D&md5=06f6a142ee1062b7de5055789120bdecCAS | open url image1

Kohaya, N., Fujiwara, K., Ito, J., and Kashiwazaki, N. (2013). Generation of live offspring from vitrified mouse oocytes of C57BL/6J strain. PLoS One 8, e58063.
Generation of live offspring from vitrified mouse oocytes of C57BL/6J strain.CrossRef | 1:CAS:528:DC%2BC3sXks1Wgurw%3D&md5=0581cf2d57388eaadddd2a2145c748a4CAS | open url image1

Kon, N., Kobayashi, Y., Li, M., Brooks, C., Ludwig, T., and Gu, W. (2010). Inactivation of HAUSP in vivo modulates p53 function. Oncogene 29, 1270–1279.
Inactivation of HAUSP in vivo modulates p53 function.CrossRef | 1:CAS:528:DC%2BD1MXhsV2gtrnK&md5=6ff26a11f2f09362aa9d0bc72f477d24CAS | open url image1

Kuleshova, L. L., and Lopata, A. (2002). Vitrification can be more favorable than slow cooling. Fertil. Steril. 78, 449–454.
Vitrification can be more favorable than slow cooling.CrossRef | open url image1

Kuwayama, M., Vajta, G., Kato, O., and Leibo, S. P. (2005). Highly efficient vitrification method for cryopreservation of human oocytes. Reprod. Biomed. Online 11, 300–308.
Highly efficient vitrification method for cryopreservation of human oocytes.CrossRef | open url image1

Kuzmany, A., Havlicek, V., Wrenzycki, C., Wilkening, S., Brem, G., and Besenfelder, U. (2011). Expression of mRNA, before and after freezing, in bovine blastocysts cultured under different conditions. Theriogenology 75, 482–494.
Expression of mRNA, before and after freezing, in bovine blastocysts cultured under different conditions.CrossRef | 1:CAS:528:DC%2BC3MXjs1Knuw%3D%3D&md5=996d3fcdd35b0d3e202d1521da3ecfd4CAS | open url image1

Lee, H. H., Lee, H. J., Kim, H. J., Lee, J. H., Ko, Y., Kim, S. M., Lee, J. R., Suh, C. S., and Kim, S. H. (2015). Effects of antifreeze proteins on the vitrification of mouse oocytes: comparison of three different antifreeze proteins. Hum. Reprod. 30, 2110–2119.
Effects of antifreeze proteins on the vitrification of mouse oocytes: comparison of three different antifreeze proteins.CrossRef | open url image1

Liang, S., Yuan, B., Kwon, J.-W., Ahn, M., Cui, X.-S., Bang, J. K., and Kim, N.-H. (2016a). Effect of antifreeze glycoprotein 8 supplementation during vitrification on the developmental competence of bovine oocytes. Theriogenology 86, 485–494.e1.
Effect of antifreeze glycoprotein 8 supplementation during vitrification on the developmental competence of bovine oocytes.CrossRef | 1:CAS:528:DC%2BC28XjtFChsb4%3D&md5=fb9bd9ebfd1eeca3219fd27a6a7d9448CAS | open url image1

Liang, S., Zhao, M.-H., Guo, J., Choi, J.-w., Kim, N.-H., and Cui, X.-S. (2016b). Polo-like kinase 4 regulates spindle and actin assembly in meiosis and influence of early embryonic development in bovine oocytes. Theriogenology 85, 754–761.e1.
Polo-like kinase 4 regulates spindle and actin assembly in meiosis and influence of early embryonic development in bovine oocytes.CrossRef | 1:CAS:528:DC%2BC2MXhslKgtrvJ&md5=5d86420ebc4dfa0b75f3c60dd164f178CAS | open url image1

Liu, W.-M., Pang, R. T., Cheong, A. W., Ng, E. H., Lao, K., Lee, K.-F., and Yeung, W. S. (2012). Involvement of microRNA lethal-7a in the regulation of embryo implantation in mice. PLoS One 7, e37039.
Involvement of microRNA lethal-7a in the regulation of embryo implantation in mice.CrossRef | 1:CAS:528:DC%2BC38XnvFaitrw%3D&md5=56165fa72daccd61c571a3ad3f2bd167CAS | open url image1

Madura, J. D., Baran, K., and Wierzbicki, A. (2000). Molecular recognition and binding of thermal hysteresis proteins to ice. J. Mol. Recognit. 13, 101–113.
Molecular recognition and binding of thermal hysteresis proteins to ice.CrossRef | 1:CAS:528:DC%2BD3cXjtFWhsLY%3D&md5=9c42d35b4a117d842d2f345d0aae23cfCAS | open url image1

Makarevich, A. V., Kubovičová, E., Popelková, M., Fabian, D., Čikoš, Š., Pivko, J., and Chrenek, P. (2010). Several aspects of animal embryo cryopreservation: anti-freeze protein (AFP) as a potential cryoprotectant. Zygote 18, 145–153.
Several aspects of animal embryo cryopreservation: anti-freeze protein (AFP) as a potential cryoprotectant.CrossRef | 1:CAS:528:DC%2BC3cXktlSit7w%3D&md5=61adc08bd3838c0bcd58c8847859f106CAS | open url image1

Pereira, R. M., and Marques, C. C. (2008). Animal oocyte and embryo cryopreservation. Cell Tissue Bank. 9, 267–277.
Animal oocyte and embryo cryopreservation.CrossRef | 1:STN:280:DC%2BD1cjksFWlsw%3D%3D&md5=b436015dc62b733654257677a34d09ccCAS | open url image1

Ptak, G., Zacchini, F., Czernik, M., Fidanza, A., Palmieri, C., Della Salda, L., Scapolo, P. A., and Loi, P. (2012). A short exposure to polychlorinated biphenyls deregulates cellular autophagy in mammalian blastocyst in vitro. Hum. Reprod. 27, 1034–1042.
A short exposure to polychlorinated biphenyls deregulates cellular autophagy in mammalian blastocyst in vitro.CrossRef | 1:CAS:528:DC%2BC38XksVarsb8%3D&md5=22f8f08fd6dd15b65e9e42f66f8cd564CAS | open url image1

Saragusty, J., and Arav, A. (2011). Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction 141, 1–19.
Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification.CrossRef | 1:CAS:528:DC%2BC3MXisVehsrc%3D&md5=c0204284ea639a5b4f5ad2fcb87c6fb3CAS | open url image1

Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675.
NIH Image to ImageJ: 25 years of image analysis.CrossRef | 1:CAS:528:DC%2BC38XhtVKntb7P&md5=951318dfcea14da7f3b365390578d9e4CAS | open url image1

Stachecki, J. J., Yelian, F. D., Leach, R. E., and Armant, D. R. (1994). Mouse blastocyst outgrowth and implantation rates following exposure to ethanol or A23187 during culture in vitro. J. Reprod. Fertil. 101, 611–617.
Mouse blastocyst outgrowth and implantation rates following exposure to ethanol or A23187 during culture in vitro.CrossRef | 1:CAS:528:DyaK2cXlvFyhu70%3D&md5=94eb30cf62e0a3d6cf23021479ef866aCAS | open url image1

Tachibana, Y., Fletcher, G. L., Fujitani, N., Tsuda, S., Monde, K., and Nishimura, S. I. (2004). Antifreeze glycoproteins: elucidation of the structural motifs that are essential for antifreeze activity. Angew. Chem. Int. Ed. Engl. 116, 874–880.
Antifreeze glycoproteins: elucidation of the structural motifs that are essential for antifreeze activity.CrossRef | open url image1

Vajta, G. (2000). Vitrification of the oocytes and embryos of domestic animals. Anim. Reprod. Sci. 60–61, 357–364.
Vitrification of the oocytes and embryos of domestic animals.CrossRef | open url image1

Venketesh, S., and Dayananda, C. (2008). Properties, potentials, and prospects of antifreeze proteins. Crit. Rev. Biotechnol. 28, 57–82.
Properties, potentials, and prospects of antifreeze proteins.CrossRef | 1:CAS:528:DC%2BD1cXislGks7k%3D&md5=bf9374b52037314207199d797ebe31ceCAS | open url image1

Wang, J.-H. (2000). A comprehensive evaluation of the effects and mechanisms of antifreeze proteins during low-temperature preservation. Cryobiology 41, 1–9.
A comprehensive evaluation of the effects and mechanisms of antifreeze proteins during low-temperature preservation.CrossRef | 1:CAS:528:DC%2BD3cXmvFehurk%3D&md5=a11d22cc5c4260f8bdcfd03e181bb49eCAS | open url image1

Wen, Y., Zhao, S., Chao, L., Yu, H., Song, C., Shen, Y., Chen, H., and Deng, X. (2014). The protective role of antifreeze protein 3 on the structure and function of mature mouse oocytes in vitrification. Cryobiology 69, 394–401.
The protective role of antifreeze protein 3 on the structure and function of mature mouse oocytes in vitrification.CrossRef | 1:CAS:528:DC%2BC2cXhs1KmtLzE&md5=6b2f19f02e16ce904bb8247d04dafc59CAS | open url image1

Wilding, M., Dale, B., Marino, M., di Matteo, L., Alviggi, C., Pisaturo, M. L., Lombardi, L., and De Placido, G. (2001). Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909–917.
Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos.CrossRef | 1:STN:280:DC%2BD3MvitlCktw%3D%3D&md5=c61663a515f0938535b09bbb474acfa0CAS | open url image1

Wilmut, I., and Rowson, L. (1973). Experiments on the low-temperature preservation of cow embryos. Vet. Rec. 92, 686–690.
Experiments on the low-temperature preservation of cow embryos.CrossRef | 1:STN:280:DyaE3s3ltVOquw%3D%3D&md5=0aedeecfcc9598e0a359a7a2540c9c04CAS | open url image1

Yang, M. Y., and Rajamahendran, R. (2002). Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim. Reprod. Sci. 70, 159–169.
Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro.CrossRef | 1:CAS:528:DC%2BD38Xis1egu7c%3D&md5=8d96aa3241e392c9db2199ed3bd2754bCAS | open url image1

Zbikowska, H. M. (2003). Fish can be first – advances in fish transgenesis for commercial applications. Transgenic Res. 12, 379–389.
Fish can be first – advances in fish transgenesis for commercial applications.CrossRef | 1:CAS:528:DC%2BD3sXks1Cnt7Y%3D&md5=5fd48cf1ff8a2df68f57824185112ffbCAS | open url image1



Supplementary MaterialSupplementary Material (6.9 MB) Export Citation

View Altmetrics