Cryoprotectant role of exopolysaccharide of Pseudomonas sp. ID1 in the vitrification of IVM cow oocytes
Núria Arcarons A , Meritxell Vendrell-Flotats A B , Marc Yeste C , Elena Mercade D , Manel López-Béjar B and Teresa Mogas A EA Department of Animal Medicine and Surgery, Autonomous University of Barcelona, Travessera dels Turons s/n, E-08193, Cerdanyola del Vallès (Barcelona), Spain.
B Department of Animal Health and Anatomy, Autonomous University of Barcelona, Travessera dels Turons s/n, E-08193, Cerdanyola del Vallès (Barcelona), Spain.
C Department of Biology, Institute of Food and Agricultural Technology, University of Girona, Girona, C/ Maria Aurèlia Campany 69, Campus Montilivi, E-17003 Girona, Spain.
D Department de Biology, Health and Environment, Microbiology Section, University of Barcelona, E-08028, Barcelona, Spain.
E Corresponding author. Email: teresa.mogas@uab.cat
Reproduction, Fertility and Development 31(9) 1507-1519 https://doi.org/10.1071/RD18447
Submitted: 28 May 2018 Accepted: 2 April 2019 Published: 16 May 2019
Abstract
Biological molecules isolated from organisms that live under subzero conditions could be used to protect oocytes from cryoinjuries suffered during cryopreservation. This study examined the cryoprotectant role of exopolysaccharides of Pseudomonas sp. ID1 (EPS ID1) in the vitrification of prepubertal and adult cow oocytes. IVM oocytes were vitrified and warmed in media supplemented with 0, 1, 10, 100 or 1000 µg mL−1 EPS ID1. After warming, oocytes were fertilised and embryo development, spindle morphology and the expression of several genes in Day 8 blastocysts were assessed. Vitrification led to significantly lower proportion of prepubertal oocytes exhibiting a normal spindle configuration. In fresh control oocytes and most groups of vitrified adult oocytes, similar percentages of oocytes with a normal spindle configuration were observed. Percentages of Day 8 blastocysts were similar for prepubertal oocytes vitrified in the absence or presence of 1 or 10 µg mL−1 EPS ID1 and for adult oocytes vitrified in the presence of 10 µg mL−1 EPS ID1 compared with non-vitrified oocytes. EPS ID1 supplementation had no effect on solute carrier family 2 member 3 (SLC2A3), ubiquitin-conjugating enzyme E2A (UBE2A) and histone deacetylase 1 (HDAC1) expression in Day 8 blastocysts form adult oocytes. However, supplementation with 10 and 100 µg mL−1 EPS ID1 led to increased expression of genes involved in epigenetic modifications (DNA methyltransferase 3 alpha (DNMT3A) and K (lysine) acetyltransferase 2A (KAT2A)) and apoptosis (BCL2 associated X apoptosis regulator (BAX) and BCL2-like 1 (BCL2L1)). The lowest BAX : BCL2L1 ratio was found in the 10 µg mL−1 EPS ID1-supplemented group. The results suggest that 10 µg mL−1 EPS ID1 added to vitrification and warming media may help protect bovine oocytes against cryodamage.
Additional keywords: calf, chromosomes, cryoprotective agents, embryo development, gene expression regulation, microtubule configuration.
References
Akiyama, T., Nagata, M., and Aoki, F. (2006). Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc. Natl Acad. Sci. USA 103, 7339–7344.| Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice.Crossref | GoogleScholarGoogle Scholar | 16651529PubMed |
Albarracín, J. L., Morató, R., Rojas, C., and Mogas, T. (2005). Effects of vitrification in open pulled straws on the cytology of in vitro matured prepubertal and adult bovine oocytes. Theriogenology 63, 890–901.
| Effects of vitrification in open pulled straws on the cytology of in vitro matured prepubertal and adult bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 15629805PubMed |
Arav, A. (2014). Cryopreservation of oocytes and embryos. Theriogenology 81, 96–102.
| Cryopreservation of oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 24274414PubMed |
Arcarons, N., Morato, R., Vendrell, M., Yeste, M., Lopez-Bejar, M., Rajapaksha, K., Anzar, M., and Mogas, T. (2017). Cholesterol added prior to vitrification on the cryotolerance of immature and in vitro matured bovine oocytes. PLoS One 12, e0184714.
| Cholesterol added prior to vitrification on the cryotolerance of immature and in vitro matured bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 28910399PubMed |
Baker, M. G., Lalonde, S. V., Konhauser, K. O., and Foght, J. M. (2010). Role of extracellular polymeric substances in the surface chemical reactivity of Hymenobacter aerophilus, a psychrotolerant bacterium. Appl. Environ. Microbiol. 76, 102–109.
| Role of extracellular polymeric substances in the surface chemical reactivity of Hymenobacter aerophilus, a psychrotolerant bacterium.Crossref | GoogleScholarGoogle Scholar | 19915039PubMed |
Balasubramanian, S., Son, W. J., Kumar, B. M., Ock, S. A., Yoo, J. G., Im, G. S., Choe, S. Y., and Rho, G. J. (2007). Expression pattern of oxygen and stress-responsive gene transcripts at various developmental stages of in vitro and in vivo preimplantation bovine embryos. Theriogenology 68, 265–275.
| Expression pattern of oxygen and stress-responsive gene transcripts at various developmental stages of in vitro and in vivo preimplantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 17559922PubMed |
Bar Dolev, M., Bernheim, R., Guo, S., Davies, P. L., and Braslavsky, I. (2016). Putting life on ice: bacteria that bind to frozen water. J. R. Soc. Interface 13, .
| Putting life on ice: bacteria that bind to frozen water.Crossref | GoogleScholarGoogle Scholar | 27534698PubMed |
Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutierrez-Adan, A. (2010). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc. Natl Acad. Sci. USA 107, 3394–3399.
| Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 20133684PubMed |
Bó, G., and Mapletoft, R. J. (2013). Evaluation and classification of bovine embryos. Anim. Reprod. 10, 344–348.
Carillo, S., Casillo, A., Pieretti, G., Parrilli, E., Sannino, F., Bayer-Giraldi, M., Cosconati, S., Novellino, E., Ewert, M., Deming, J. W., Lanzetta, R., Marino, G., Parrilli, M., Randazzo, A., Tutino, M. L., and Corsaro, M. M. (2015). A unique capsular polysaccharide structure from the psychrophilic marine bacterium Colwellia psychrerythraea 34H that mimics antifreeze (glyco)proteins. J. Am. Chem. Soc. 137, 179–189.
| A unique capsular polysaccharide structure from the psychrophilic marine bacterium Colwellia psychrerythraea 34H that mimics antifreeze (glyco)proteins.Crossref | GoogleScholarGoogle Scholar | 25525681PubMed |
Carrión, O., Delgado, L., and Mercade, E. (2015). New emulsifying and cryoprotective exopolysaccharide from Antarctic Pseudomonas sp. ID1. Carbohydr. Polym. 117, 1028–1034.
| New emulsifying and cryoprotective exopolysaccharide from Antarctic Pseudomonas sp. ID1.Crossref | GoogleScholarGoogle Scholar | 25498731PubMed |
Chaves, D. F., Campelo, I. S., Silva, M. M., Bhat, M. H., Teixeira, D. I., Melo, L. M., Souza-Fabjan, J. M., Mermillod, P., and Freitas, V. J. (2016). The use of antifreeze protein type III for vitrification of in vitro matured bovine oocytes. Cryobiology 73, 324–328.
| The use of antifreeze protein type III for vitrification of in vitro matured bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 27729221PubMed |
Chen, H., Zhang, L., Deng, T., Zou, P., Wang, Y., Quan, F., and Zhang, Y. (2016). Effects of oocyte vitrification on epigenetic status in early bovine embryos. Theriogenology 86, 868–878.
| Effects of oocyte vitrification on epigenetic status in early bovine embryos.Crossref | GoogleScholarGoogle Scholar | 27068359PubMed |
Daley, M. E., and Sykes, B. D. (2003). The role of side chain conformational flexibility in surface recognition by Tenebrio molitor antifreeze protein. Protein Sci. 12, 1323–1331.
| The role of side chain conformational flexibility in surface recognition by Tenebrio molitor antifreeze protein.Crossref | GoogleScholarGoogle Scholar | 12824479PubMed |
Davies, P. L. (2014). Ice-binding proteins: a remarkable diversity of structures for stopping and starting ice growth. Trends Biochem. Sci. 39, 548–555.
| Ice-binding proteins: a remarkable diversity of structures for stopping and starting ice growth.Crossref | GoogleScholarGoogle Scholar | 25440715PubMed |
de Paz, P., Sanchez, A. J., De la Fuente, J., Chamorro, C. A., Alvarez, M., Anel, E., and Anel, L. (2001). Ultrastructural and cytochemical comparison between calf and cow oocytes. Theriogenology 55, 1107–1116.
| Ultrastructural and cytochemical comparison between calf and cow oocytes.Crossref | GoogleScholarGoogle Scholar | 11322238PubMed |
Dreischmeier, K., Budke, C., Wiehemeier, L., Kottke, T., and Koop, T. (2017). Boreal pollen contain ice-nucleating as well as ice-binding ‘antifreeze’ polysaccharides. Sci. Rep. 7, 41890.
| Boreal pollen contain ice-nucleating as well as ice-binding ‘antifreeze’ polysaccharides.Crossref | GoogleScholarGoogle Scholar | 28157236PubMed |
Duan, X. X., Ou, J. S., Li, Y., Su, J. J., Ou, C., Yang, C., Yue, H. F., and Ban, K. C. (2005). Dynamic expression of apoptosis-related genes during development of laboratory hepatocellular carcinoma and its relation to apoptosis. World J. Gastroenterol. 11, 4740–4744.
| Dynamic expression of apoptosis-related genes during development of laboratory hepatocellular carcinoma and its relation to apoptosis.Crossref | GoogleScholarGoogle Scholar | 16094721PubMed |
Ewert, M., and Deming, J. W. (2013). Sea ice microorganisms: environmental constraints and extracellular responses. Biology (Basel) 2, 603–628.
| Sea ice microorganisms: environmental constraints and extracellular responses.Crossref | GoogleScholarGoogle Scholar | 24832800PubMed |
Freitas, F., Alves, V. D., and Reis, M. A. (2011). Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol. 29, 388–398.
| Advances in bacterial exopolysaccharides: from production to biotechnological applications.Crossref | GoogleScholarGoogle Scholar | 21561675PubMed |
Gandolfi, F., Milanesi, E., Pocar, P., Luciano, A. M., Brevini, T. A., Acocella, F., Lauria, A., and Armstrong, D. T. (1998). Comparative analysis of calf and cow oocytes during in vitro maturation. Mol. Reprod. Dev. 49, 168–175.
| Comparative analysis of calf and cow oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 9444659PubMed |
Huang, J. C., Yan, L. Y., Lei, Z. L., Miao, Y. L., Shi, L. H., Yang, J. W., Wang, Q., Ouyang, Y. C., Sun, Q. Y., and Chen, D. Y. (2007). Changes in histone acetylation during postovulatory aging of mouse oocyte. Biol. Reprod. 77, 666–670.
| Changes in histone acetylation during postovulatory aging of mouse oocyte.Crossref | GoogleScholarGoogle Scholar | 17582009PubMed |
Hwang, I. S., and Hochi, S. (2014). Recent progress in cryopreservation of bovine oocytes. BioMed Res. Int. 2014, 570647.
| Recent progress in cryopreservation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 25401106PubMed |
Jo, J. W., Jee, B. C., Lee, J. R., and Suh, C. S. (2011). Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence. Fertil. Steril. 96, 1239–1245.
| Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 21917250PubMed |
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 | GoogleScholarGoogle Scholar | 22649508PubMed |
Kaneda, M., Okano, M., Hata, K., Sado, T., Tsujimoto, N., Li, E., and Sasaki, H. (2004). Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429, 900–903.
| Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting.Crossref | GoogleScholarGoogle Scholar | 15215868PubMed |
Kauffold, J., Am, H. A., Bergfeld, U., Weber, W., and Sobiraj, A. (2005). The in vitro developmental competence of oocytes from juvenile calves is related to follicular diameter. J. Reprod. Dev. 51, 325–332.
| The in vitro developmental competence of oocytes from juvenile calves is related to follicular diameter.Crossref | GoogleScholarGoogle Scholar | 16000866PubMed |
Khatir, H., Lonergan, P., Carolan, C., and Mermillod, P. (1996). Prepubertal bovine oocyte: a negative model for studying oocyte developmental competence. Mol. Reprod. Dev. 45, 231–239.
| Prepubertal bovine oocyte: a negative model for studying oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 8914082PubMed |
Kim, S. J., and Yim, J. H. (2007). Cryoprotective properties of exopolysaccharide (P-21653) produced by the Antarctic bacterium, Pseudoalteromonas arctica KOPRI 21653. J. Microbiol. 45, 510–514.
| 18176533PubMed |
Krembs, C., Eicken, H., Junge, K., and Deming, J. W. (2002). High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep Sea Res. Part I Oceanogr. Res. Pap. 49, 2163–2181.
| High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms.Crossref | GoogleScholarGoogle Scholar |
Lazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T., Niemann, H., and Galli, C. (2002). Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol. Reprod. 67, 767–775.
| Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome.Crossref | GoogleScholarGoogle Scholar | 12193383PubMed |
Ledda, S., Leoni, G., Bogliolo, L., and Naitana, S. (2001). Oocyte cryopreservation and ovarian tissue banking. Theriogenology 55, 1359–1371.
| Oocyte cryopreservation and ovarian tissue banking.Crossref | GoogleScholarGoogle Scholar | 11327689PubMed |
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 | GoogleScholarGoogle Scholar | 26202918PubMed |
Li, L., Zheng, P., and Dean, J. (2010). Maternal control of early mouse development. Development 137, 859–870.
| Maternal control of early mouse development.Crossref | GoogleScholarGoogle Scholar | 20179092PubMed |
Liang, S., Yuan, B., Kwon, J. W., Ahn, M., Cui, X. S., Bang, J. K., and Kim, N. H. (2016). 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 | GoogleScholarGoogle Scholar | 26948296PubMed |
Liu, S. B., Chen, X. L., He, H. L., Zhang, X. Y., Xie, B. B., Yu, Y., Chen, B., Zhou, B. C., and Zhang, Y. Z. (2013). Structure and ecological roles of a novel exopolysaccharide from the arctic sea ice bacterium Pseudoalteromonas sp. strain SM20310. Appl. Environ. Microbiol. 79, 224–230.
| Structure and ecological roles of a novel exopolysaccharide from the arctic sea ice bacterium Pseudoalteromonas sp. strain SM20310.Crossref | GoogleScholarGoogle Scholar | 23087043PubMed |
Lundheim, R. (2002). Physiological and ecological significance of biological ice nucleators. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 937–943.
| Physiological and ecological significance of biological ice nucleators.Crossref | GoogleScholarGoogle Scholar | 12171657PubMed |
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 | GoogleScholarGoogle Scholar | 10822254PubMed |
Mandawala, A. A., Harvey, S. C., Roy, T. K., and Fowler, K. E. (2016). Cryopreservation of animal oocytes and embryos: current progress and future prospects. Theriogenology 86, 1637–1644.
| Cryopreservation of animal oocytes and embryos: current progress and future prospects.Crossref | GoogleScholarGoogle Scholar | 27555525PubMed |
Morató, R., Izquierdo, D., Paramio, M. T., and Mogas, T. (2008). Cryotops versus open-pulled straws (OPS) as carriers for the cryopreservation of bovine oocytes: effects on spindle and chromosome configuration and embryo development. Cryobiology 57, 137–141.
| Cryotops versus open-pulled straws (OPS) as carriers for the cryopreservation of bovine oocytes: effects on spindle and chromosome configuration and embryo development.Crossref | GoogleScholarGoogle Scholar | 18680737PubMed |
Mullen, S. F., and Fahy, G. M. (2012). A chronologic review of mature oocyte vitrification research in cattle, pigs, and sheep. Theriogenology 78, 1709–1719.
| A chronologic review of mature oocyte vitrification research in cattle, pigs, and sheep.Crossref | GoogleScholarGoogle Scholar | 22968034PubMed |
Nichols, C. M., Lardiere, S. G., Bowman, J. P., Nichols, P. D., Gibson, J. A. E., and Guézennec, J. (2005). Chemical characterization of exopolysaccharides from Antarctic marine bacteria. Microb. Ecol. 49, 578–589.
| Chemical characterization of exopolysaccharides from Antarctic marine bacteria.Crossref | GoogleScholarGoogle Scholar | 16052372PubMed |
O’Doherty, A. M., O’Shea, L. C., and Fair, T. (2012). Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biol. Reprod. 86, 67.
| Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins.Crossref | GoogleScholarGoogle Scholar | 22088914PubMed |
Opiela, J., Katska-Ksiazkiewicz, L., Lipinski, D., Slomski, R., Bzowska, M., and Rynska, B. (2008). Interactions among activity of glucose-6-phosphate dehydrogenase in immature oocytes, expression of apoptosis-related genes Bcl-2 and Bax, and developmental competence following IVP in cattle. Theriogenology 69, 546–555.
| Interactions among activity of glucose-6-phosphate dehydrogenase in immature oocytes, expression of apoptosis-related genes Bcl-2 and Bax, and developmental competence following IVP in cattle.Crossref | GoogleScholarGoogle Scholar | 18242680PubMed |
Oude Vrielink, A. S., Aloi, A., Olijve, L. L., and Voets, I. K. (2016). Interaction of ice binding proteins with ice, water and ions. Biointerphases 11, 018906.
| Interaction of ice binding proteins with ice, water and ions.Crossref | GoogleScholarGoogle Scholar | 26787386PubMed |
Rizos, D., Ward, F., Boland, M. P., and Lonergan, P. (2001). Effect of culture system on the yield and quality of bovine blastocysts as assessed by survival after vitrification. Theriogenology 56, 1–16.
| Effect of culture system on the yield and quality of bovine blastocysts as assessed by survival after vitrification.Crossref | GoogleScholarGoogle Scholar | 11467505PubMed |
Shirazi, A., Naderi, M. M., Hassanpour, H., Heidari, M., Borjian, S., Sarvari, A., and Akhondi, M. M. (2016). The effect of ovine oocyte vitrification on expression of subset of genes involved in epigenetic modifications during oocyte maturation and early embryo development. Theriogenology 86, 2136–2146.
| The effect of ovine oocyte vitrification on expression of subset of genes involved in epigenetic modifications during oocyte maturation and early embryo development.Crossref | GoogleScholarGoogle Scholar | 27501872PubMed |
Spinaci, M., Vallorani, C., Bucci, D., Tamanini, C., Porcu, E., and Galeati, G. (2012). Vitrification of pig oocytes induces changes in histone H4 acetylation and histone H3 lysine 9 methylation (H3K9). Vet. Res. Commun. 36, 165–171.
| Vitrification of pig oocytes induces changes in histone H4 acetylation and histone H3 lysine 9 methylation (H3K9).Crossref | GoogleScholarGoogle Scholar | 22706936PubMed |
Sprícigo, J., Arcarons, N., Dode, M., Mogas, T., and Morató, R. (2015). Spindle configuration and DNA fragmentation of vitrified bovine oocytes after IVM with l-carnitine and/or resveratrol. Reprod. Fertil. Dev. 27, 115–116.
| Spindle configuration and DNA fragmentation of vitrified bovine oocytes after IVM with l-carnitine and/or resveratrol.Crossref | GoogleScholarGoogle Scholar |
Sprícigo, J. F., Morató, R., Arcarons, N., Yeste, M., Dode, M. A., López-Bejar, M., and Mogas, T. (2017). Assessment of the effect of adding l-carnitine and/or resveratrol to maturation medium before vitrification on in vitro-matured calf oocytes. Theriogenology 89, 47–57.
| Assessment of the effect of adding l-carnitine and/or resveratrol to maturation medium before vitrification on in vitro-matured calf oocytes.Crossref | GoogleScholarGoogle Scholar | 28043370PubMed |
Strahl, B. D., and Allis, C. D. (2000). The language of covalent histone modifications. Nature 403, 41–45.
| The language of covalent histone modifications.Crossref | GoogleScholarGoogle Scholar | 10638745PubMed |
Succu, S., Leoni, G. G., Berlinguer, F., Madeddu, M., Bebbere, D., Mossa, F., Bogliolo, L., Ledda, S., and Naitana, S. (2007). Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes. Theriogenology 68, 107–114.
| Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes.Crossref | GoogleScholarGoogle Scholar | 17537497PubMed |
Succu, S., Bebbere, D., Bogliolo, L., Ariu, F., Fois, S., Leoni, G. G., Berlinguer, F., Naitana, S., and 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.
| Vitrification of in vitro matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance.Crossref | GoogleScholarGoogle Scholar | 17886274PubMed |
Suo, L., Meng, Q., Pei, Y., Fu, X., Wang, Y., Bunch, T. D., and Zhu, S. (2010). Effect of cryopreservation on acetylation patterns of lysine 12 of histone H4 (acH4K12) in mouse oocytes and zygotes. J. Assist. Reprod. Genet. 27, 735–741.
| Effect of cryopreservation on acetylation patterns of lysine 12 of histone H4 (acH4K12) in mouse oocytes and zygotes.Crossref | GoogleScholarGoogle Scholar | 20838874PubMed |
Walters, K. R., Serianni, A. S., Sformo, T., Barnes, B. M., and Duman, J. G. (2009). A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. Proc. Natl Acad. Sci. USA 106, 20210–20215.
| A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides.Crossref | GoogleScholarGoogle Scholar | 19934038PubMed |
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 | GoogleScholarGoogle Scholar | 25263096PubMed |
Wilson, Z. E., and Brimble, M. A. (2009). Molecules derived from the extremes of life. Nat. Prod. Rep. 26, 44–71.
| Molecules derived from the extremes of life.Crossref | GoogleScholarGoogle Scholar | 19374122PubMed |
Yamashita, Y., Kawahara, H., and Obata, H. (2002). Identification of a novel anti-ice-nucleating polysaccharide from Bacillus thuringiensis YY529. Biosci. Biotechnol. Biochem. 66, 948–954.
| Identification of a novel anti-ice-nucleating polysaccharide from Bacillus thuringiensis YY529.Crossref | GoogleScholarGoogle Scholar | 12092845PubMed |
Yan, L. Y., Yan, J., Qiao, J., Zhao, P. L., and Liu, P. (2010). Effects of oocyte vitrification on histone modifications. Reprod. Fertil. Dev. 22, 920–925.
| Effects of oocyte vitrification on histone modifications.Crossref | GoogleScholarGoogle Scholar | 20591326PubMed |
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 | GoogleScholarGoogle Scholar | 11943486PubMed |
Yeh, Y., and Feeney, R. E. (1996). Antifreeze proteins: structures and mechanisms of function. Chem. Rev. 96, 601–618.
| Antifreeze proteins: structures and mechanisms of function.Crossref | GoogleScholarGoogle Scholar | 11848766PubMed |
Zachariassen, K. E., and Kristiansen, E. (2000). Ice nucleation and antinucleation in nature. Cryobiology 41, 257–279.
| Ice nucleation and antinucleation in nature.Crossref | GoogleScholarGoogle Scholar | 11222024PubMed |
Zander-Fox, D., Cashman, K. S., and Lane, M. (2013). The presence of 1 mM glycine in vitrification solutions protects oocyte mitochondrial homeostasis and improves blastocyst development. J. Assist. Reprod. Genet. 30, 107–116.
| The presence of 1 mM glycine in vitrification solutions protects oocyte mitochondrial homeostasis and improves blastocyst development.Crossref | GoogleScholarGoogle Scholar | 23248076PubMed |