Ice formation and its elimination in cryopreservation of oocytes

Fahy, G. M. & Wowk, B. Principles of cryopreservation by vitrification. In Cryopreservation and Freeze-Drying Protocols Vol. 1257 (eds Wolkers, W. F. & Oldenhof, H.) 21–82 (Springer, 2015).Chapter 

Google Scholar 
Pegg, D. E. Principles of cryopreservation. In Cryopreservation and Freeze-Drying Protocols (eds Wolkers, W. F. & Oldenhof, H.) 3–19 (Springer, 2015). Chapter 

Google Scholar 
Hubel, A. & Skubitz, A. P. N. Principles of cryopreservation. In Biobanking of Human Biospecimens (eds Hainaut, P. et al.) 1–21 (Springer, 2017). 
Google Scholar 
Nagy, Z. P., Nel-Themaat, L., Chang, C.-C., Shapiro, D. B. & Berna, D. P. Cryopreservation of eggs. In Human Fertility: Methods and Protocols (eds Rosenwaks, Z. & Wassarman, P. M.) 439–454 (Springer, 2014). Chapter 

Google Scholar 
Arav, A. & Natan, Y. Vitrification of oocytes: From basic science to clinical application. In Oocyte Biology in Fertility Preservation Vol. 761 (ed. Kim, S. S.) 69–83 (Springer, 2013).Chapter 

Google Scholar 
Chian, R.-C., Wang, Y. & Li, Y.-R. Oocyte vitrification: Advances, progress and future goals. J. Assist. Reprod. Genet. 31, 411–420 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Mandawala, A. A., Harvey, S. C., Roy, T. K. & Fowler, K. E. Cryopreservation of animal oocytes and embryos: Current progress and future prospects. Theriogenology 86, 1637–1644 (2016).Article 
CAS 
PubMed 

Google Scholar 
Rosenwaks, Z. & Wassarman, P. Human Fertility (Springer, 2014).Book 

Google Scholar 
Hasler, J. F. Factors affecting frozen and fresh embryo transfer pregnancy rates in cattle. Theriogenology 56, 1401–1415 (2001).Article 
CAS 
PubMed 

Google Scholar 
Hasler, J. F. Forty years of embryo transfer in cattle: A review focusing on the journal Theriogenology, the growth of the industry in North America, and personal reminisces. Theriogenology 81, 152–169 (2014).Article 
PubMed 

Google Scholar 
Martinez, A. G., Brogliatti, G. M., Valcarcel, A. & de las Heras, M. A. Pregnancy rates after transfer of frozen bovine embryos: A field trial. Theriogenology 58, 963–972 (2002).Article 
CAS 
PubMed 

Google Scholar 
Zhan, L., Li, M., Hays, T. & Bischof, J. Cryopreservation method for Drosophila melanogaster embryos. Nat. Commun. 12, 2412 (2021).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Xingzhu, D. et al. Cryopreservation of porcine embryos: Recent updates and progress. Biopreserv. Biobank. 19, 210–218 (2021).Article 
PubMed 

Google Scholar 
Andrabi, S. M. H. & Maxwell, W. M. C. A review on reproductive biotechnologies for conservation of endangered mammalian species. Anim. Reprod. Sci. 99, 223–243 (2007).Article 
CAS 
PubMed 

Google Scholar 
Holt, W. V. & Brown, J. L. Reproductive sciences in animal conservation. Adv. Exp. Med. Biol. 753, 3–14 (2014).Article 
PubMed 

Google Scholar 
Lee, S., Iwasaki, Y., Shikina, S. & Yoshizaki, G. Generation of functional eggs and sperm from cryopreserved whole testes. Proc. Natl. Acad. Sci. 110, 1640–1645 (2013).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Comizzoli, P. & Holt, W. V. Recent advances and prospects in germplasm preservation of rare and endangered species. In Reproductive Sciences in Animal Conservation Vol. 753 (eds Holt, W. V. et al.) 331–356 (Springer, 2014).Chapter 

Google Scholar 
Huang, J. & Bartell, L. S. Kinetics of homogeneous nucleation in the freezing of large water clusters. J. Phys. Chem. 99, 3924–3931 (1995).Article 
CAS 

Google Scholar 
Manka, A. et al. Freezing water in no-man’s land. Phys. Chem. Chem. Phys. 14, 4505 (2012).Article 
CAS 
PubMed 

Google Scholar 
Hey, J. M. & MacFarlane, D. R. Crystallization of ice in aqueous solutions of glycerol and dimethyl sulfoxide 2: Ice crystal growth kinetics. Cryobiology 37, 119–130 (1998).Article 
CAS 
PubMed 

Google Scholar 
Wang, Q., Zhao, L., Li, C. & Cao, Z. The decisive role of free water in determining homogenous ice nucleation behavior of aqueous solutions. Sci. Rep. 6, 26831 (2016).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Szurek, E. A. & Eroglu, A. Comparison and avoidance of toxicity of penetrating cryoprotectants. PLoS ONE 6, e27604 (2011).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Best, B. P. Cryoprotectant toxicity: Facts, issues, and questions. Rejuvenation Res. 18, 422–436 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Arakawa, T., Carpenter, J. F., Kita, Y. A. & Crowe, J. H. The basis for toxicity of certain cryoprotectants: A hypothesis. Cryobiology 27, 401–415 (1990).Article 
CAS 

Google Scholar 
Yamada, C. et al. Immature bovine oocyte cryopreservation: Comparison of different associations with ethylene glycol, glycerol and dimethylsulfoxide. Anim. Reprod. Sci. 99, 384–388 (2007).Article 
CAS 
PubMed 

Google Scholar 
Privalov, P. L. Cold denaturation of proteins. Crit. Rev. Biochem. Mol. Biol. 25, 281–306 (1990).Article 
CAS 
PubMed 

Google Scholar 
Fayter, A. E. R., Hasan, M., Congdon, T. R., Kontopoulou, I. & Gibson, M. I. Ice recrystallisation inhibiting polymers prevent irreversible protein aggregation during solvent-free cryopreservation as additives and as covalent polymer-protein conjugates. Eur. Polym. J. 140, 110036 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Fahy, G. M., Saur, J. & Williams, R. J. Physical problems with the vitrification of large biological systems. Cryobiology 27, 492–510 (1990).Article 
CAS 
PubMed 

Google Scholar 
Kasai, M. et al. Fracture damage of embryos and its prevention during vitrification and warming. Cryobiology 33, 459–464 (1996).Article 
CAS 
PubMed 

Google Scholar 
Steif, P. S., Palastro, M. C. & Rabin, Y. Analysis of the effect of partial vitrification on stress development in cryopreserved blood vessels. Med. Eng. Phys. 29, 661–670 (2007).Article 
PubMed 

Google Scholar 
Eisenberg, D. P., Steif, P. S. & Rabin, Y. On the effects of thermal history on the development and relaxation of thermo-mechanical stress in cryopreservation. Cryogenics 64, 86–94 (2014).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Seki, S. & Mazur, P. The dominance of warming rate over cooling rate in the survival of mouse oocytes subjected to a vitrification procedure. Cryobiology 59, 75–82 (2009).Article 
PubMed 
PubMed Central 

Google Scholar 
Seki, S. & Mazur, P. Ultra-rapid warming yields high survival of mouse oocytes cooled to − 196°C in dilutions of a standard vitrification solution. PLoS ONE 7, e36058 (2012).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Mazur, P. & Seki, S. Survival of mouse oocytes after being cooled in a vitrification solution to − 196°C at 95° to 70,000°C/min and warmed at 610° to 118,000°C/min: A new paradigm for cryopreservation by vitrification. Cryobiology 62, 1–7 (2011).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Seki, S., Jin, B. & Mazur, P. Extreme rapid warming yields high functional survivals of vitrified 8-cell mouse embryos even when suspended in a half-strength vitrification solution and cooled at moderate rates to − 196°C. Cryobiology 68, 71–78 (2014).Article 
PubMed 

Google Scholar 
Jin, B., Kleinhans, F. W. & Mazur, P. Survivals of mouse oocytes approach 100% after vitrification in 3-fold diluted media and ultra-rapid warming by an IR laser pulse. Cryobiology 68, 419–430 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Jin, B. & Mazur, P. High survival of mouse oocytes/embryos after vitrification without permeating cryoprotectants followed by ultra-rapid warming with an IR laser pulse. Sci. Rep. 5, 9271 (2015).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Khosla, K., Wang, Y., Hagedorn, M., Qin, Z. & Bischof, J. Gold nanorod induced warming of embryos from the cryogenic state enhances viability. ACS Nano 11, 7869–7878 (2017).Article 
CAS 
PubMed 

Google Scholar 
Zhan, L. et al. Rapid joule heating improves vitrification based cryopreservation. Nat. Commun. 13, 6017 (2022).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Huebinger, J. et al. Direct measurement of water states in cryopreserved cells reveals tolerance toward ice crystallization. Biophys. J. 110, 840–849 (2016).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Kleinhans, F. W., Guenther, J. F., Roberts, D. M. & Mazur, P. Analysis of intracellular ice nucleation in Xenopus oocytes by differential scanning calorimetry. Cryobiology 52, 128–138 (2006).Article 
CAS 
PubMed 

Google Scholar 
Mazur, P., Seki, S., Pinn, I. L., Kleinhans, F. W. & Edashige, K. Extra- and intracellular ice formation in mouse oocytes. Cryobiology 51, 29–53 (2005).Article 
CAS 
PubMed 

Google Scholar 
Seki, S. & Mazur, P. Stability of mouse oocytes at − 80 °C: The role of the recrystallization of intracellular ice. Reprod. Camb. Engl. 141, 407–415 (2011).Article 
CAS 

Google Scholar 
Moreau, D. W., Atakisi, H. & Thorne, R. E. Ice formation and solvent nanoconfinement in protein crystals. IUCrJ 6, 346–356 (2019).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Anzar, M., Grochulski, P. & Bonnet, B. Synchrotron X-ray diffraction to detect glass or ice formation in the vitrified bovine cumulus-oocyte complexes and morulae. PLoS ONE 9, e114801 (2014).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Rupp, B. Biomolecular Crystallography: Principles, Practice, and Application to Structural Biology (Garland Science, 2009).Book 

Google Scholar 
Pflugrath, J. W. Practical macromolecular cryocrystallography. Acta Crystallogr. Sect. F 71, 622–642 (2015).Article 
CAS 

Google Scholar 
Berejnov, V., Husseini, N. S., Alsaied, O. A. & Thorne, R. E. Effects of cryoprotectant concentration and cooling rate on vitrification of aqueous solutions. J. Appl. Crystallogr. 39, 244–251 (2006).Article 
ADS 
CAS 

Google Scholar 
Hartman, C. G. How large is the Mammalian egg? A review. Q. Rev. Biol. 4, 373–388 (1929).Article 

Google Scholar 
Ménézo, Y. J. & Hérubel, F. Mouse and bovine models for human IVF. Reprod. Biomed. Online 4, 170–175 (2002).Article 
PubMed 

Google Scholar 
Malkin, T. L. et al. Structure of ice crystallized from supercooled water. Proc. Natl. Acad. Sci. 109, 1041–1045 (2012).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Malkin, T. L. et al. Stacking disorder in ice I. Phys. Chem. Chem. Phys. 17, 60–76 (2015).Article 
CAS 
PubMed 

Google Scholar 
Warkentin, M. A., Sethna, J. P. & Thorne, R. E. Critical droplet theory explains the glass formability of aqueous solutions. Phys. Rev. Lett. 110, 015703 (2013).Article 
ADS 
PubMed 

Google Scholar 
Kuwayama, M. Highly efficient vitrification for cryopreservation of human oocytes and embryos: The Cryotop method. Theriogenology 67, 73–80 (2007).Article 
CAS 
PubMed 

Google Scholar 
Fortes, A. D. Accurate and precise lattice parameters of H2O and D2O ice Ih between 1.6 and 270 K from high-resolution time-of-flight neutron powder diffraction data. Acta Crystallogr. Sect. B 74, 196–216 (2018).Article 
ADS 
CAS 

Google Scholar 
Kitazato Corp. Cryotop cooling and warming rates. Kitazato. www.kitazato-ivf.com/vitrification/cryotop/.Seki, S. & Mazur, P. Effect of warming rate on the survival of vitrified mouse oocytes and on the recrystallization of intracellular ice. Biol. Reprod. 79, 727–737 (2008).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wowk, B. Thermodynamic aspects of vitrification. Cryobiology 60, 11–22 (2010).Article 
CAS 
PubMed 

Google Scholar 
Boyce, B. L., Furnish, T. A., Padilla, H. A., Van Campen, D. & Mehta, A. Detecting rare, abnormally large grains by x-ray diffraction. J. Mater. Sci. 50, 6719–6729 (2015).Article 
ADS 
CAS 

Google Scholar 
Pruppacher, H. R. Some relations between the structure of the ice-solution interface and the free growth rate of ice crystals in supercooled aqueous solutions. J. Colloid Interface Sci. 25, 285–294 (1967).Article 
ADS 
CAS 

Google Scholar 
Amir, A., Yehudit, N., Pasquale, P. & Roy, A. The effect of cryoprotectants concentration on ice crystal propagation velocity. Biopreserv. Biobank. 21, 547–553 (2023).Article 
CAS 
PubMed 

Google Scholar 
Paredes, E. & Mazur, P. The survival of mouse oocytes shows little or no correlation with the vitrification or freezing of the external medium, but the ability of the medium to vitrify is affected by its solute concentration and by the cooling rate. Cryobiology 67, 386–390 (2013).Article 
PubMed 

Google Scholar 
Hudait, A., Qiu, S., Lupi, L. & Molinero, V. Free energy contributions and structural characterization of stacking disordered ices. Phys. Chem. Chem. Phys. 18, 9544–9553 (2016).Article 
CAS 
PubMed 

Google Scholar 
Engstrom, T. et al. High-resolution single-particle cryo-EM of samples vitrified in boiling nitrogen. IUCrJ 8, 1–11 (2021).Article 

Google Scholar 
Kuwayama, M., Vajta, G., Ieda, S. & Kato, O. Comparison of open and closed methods for vitrification of human embryos and the elimination of potential contamination. Reprod. Biomed. Online 11, 608–614 (2005).Article 
PubMed 

Google Scholar 
Risco, R., Elmoazzen, H., Doughty, M., He, X. & Toner, M. Thermal performance of quartz capillaries for vitrification. Cryobiology 55, 222–229 (2007).Article 
CAS 
PubMed 

Google Scholar 
Lee, H.-J. et al. Ultra-rapid vitrification of mouse oocytes in low cryoprotectant concentrations. Reprod. Biomed. Online 20, 201–208 (2010).Article 
PubMed 

Google Scholar 
Liu, J., Lee, G. Y., Biggers, J. D., Toth, T. L. & Toner, M. Low cryoprotectant concentration rapid vitrification of mouse oocytes and embryos. Cryobiology 98, 233–238 (2021).Article 
CAS 
PubMed 

Google Scholar 
Akiyama, Y., Shinose, M., Watanabe, H., Yamada, S. & Kanda, Y. Cryoprotectant-free cryopreservation of mammalian cells by superflash freezing. Proc. Natl. Acad. Sci. 116, 7738–7743 (2019).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tyree, T. J., Dan, R. & Thorne, R. E. Density and electron density of aqueous cryoprotectant solutions at cryogenic temperatures for optimized cryoprotection and diffraction contrast. Acta Crystallogr. Sect. D 74, 471–479 (2018).Article 
ADS 
CAS 

Google Scholar 
Kriminski, S., Kazmierczak, M. & Thorne, R. E. Heat transfer from protein crystals: Implications for flash-cooling and X-ray beam heating. Acta Crystallogr. Sect. D 59, 697–708 (2003).Article 
ADS 
CAS 

Google Scholar 
Kleinhans, F. W. & Mazur, P. Physical parameters, modeling, and methodological details in using IR laser pulses to warm frozen or vitrified cells ultra-rapidly. Cryobiology 70, 195–203 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Khosla, K. et al. Characterization of laser gold nanowarming: A platform for millimeter-scale cryopreservation. Langmuir 35, 7364–7375 (2019).Article 
CAS 
PubMed 

Google Scholar 
Hopkins, J. B., Badeau, R., Warkentin, M. & Thorne, R. E. Effect of common cryoprotectants on critical warming rates and ice formation in aqueous solutions. Cryobiology 65, 169–178 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Treacy, M. M. J., Newsam, J. M. & Deem, M. W. A general recursion method for calculating diffracted intensities from crystals containing planar faults. Proc. R. Soc. A 433, 499–520 (1991).ADS 

Google Scholar 

Hot Topics

Related Articles