Biophysics of Cryopreservation

Year 2022, Volume: 25 Issue: 1, 17 - 27, 01.03.2022

Yashasvı Sharma Mona Sharma

https://doi.org/10.5541/ijot.925283

Cited By: 6

Abstract

A significant credit towards today’s scientific and medical advancements goes to the technique of cryopreservation. Cryopreservation refers to the maintenance of cellular life at subzero temperatures for a definite period of time in a state of suspended cellular metabolism. The technique has become an indispensable step in most scientific research and medical applications like assisted reproduction, transplantations, and cell-based therapies where-in it allows the long-term preservation of biological specimens like gametes, embryos, viruses, cells and tissues. Although already an extensively used technique, a significant proportion of the cryopreserved samples still incur notable damage. Ultimately this leads to a decreased post-thaw viability and proliferation. Moreover, it is also possible that events during the freezing process, provoke more serious disturbances in the preserved material with regard to its identity and functionality. Hence, with the need to use the technique more judiciously, additional studies are needed for optimizing the current cryopreservation methods in use. For this, a thorough understanding of the normal physiological changes that the cryopreserved sample undergoes and the physics of cryopreservation seems plausible. The review thus aims to unravel the current knowledge on the complex physico-chemical processes and reactions that occur during the standard cryopreservation techniques.

Keywords

cryopreservation, vitrification, freezing, thawing, biophysics

References

• Semen Freezing Past Present and Future. 4th Nexus E-bulletin.Indian Fertility Society & Origio India Initiative. 2017.
• D. E. Pegg. Principles of cryopreservation. Methods Mol Biol, 368: 39-57, 2007.
• P. Mazur. Principles of cryobiology. in Fuller, B.J., Lane, N.L., Benson, E.E. (Eds.), Life in the frozen state. CRC Press LLC, Boca Raton, FL, pp 3–65, 2004.
• The Physics of Ice: It All Begins with Nucleation. Alex Esmon 12.18.2014. Thermofisher Scientific.
• G. J. Morris, E. Acton. Controlled ice nucleation in cryopreservation – A review. Cryobiology, vol. 66, No. 2, pp.85-92, 2013.
• P. Mazur. Freezing of living cells: Mechanisms and implications, Am. J. Physiol. 247, C125–C142, 1984.
• P. Mazur, S. Leibo, E. Chu. A two-factor hypothesis of freezing injury. Evidence from hamster tissue-culture cells. Exp. Cell Res, vol. 71, No.2, pp. 345-355, 1972.
• J. E. Lovelock. The haemolysis of human red blood cells by freezing and thawing. Biochim. Biophys. Acta. Vol.10, pp. 414– 426, 1953.
• D.E. Pegg. Principles of cryopreservation. Methods Mol Biol. Vol. 1257, No. 3, pp.19, 2015.
• Principles of Cryopreservation by Vitrification Authors: Gregory M. Fahy Brian Wowk Series: Methods In Molecular Biology > Book: Cryopreservation and Freeze-Drying Protocols. 2015. Springer Protocols. Springer-Verlag New York. Humana Press. Willem F. Wolkers, Harriëtte Oldenhof (eds.).
• B. Wowk. Thermodynamic aspects of vitrification. Cryobiology. Vol. 60, No.1, pp. 11-22, 2010.
• N. Chao, I. Chiu Liao. Cryopreservation of finfish and shellfish gametes and embryos, Editor(s): Cheng-Sheng Lee, Edward M. Donaldson, Reproductive Biotechnology in Finfish Aquaculture, Elsevier, pp.161-189, 2001.
• G. M. Fahy. Biological Effects of Vitrification and Devitrification. In: D.E. Pegg, A.M. Karow (eds) The Biophysics of Organ Cryopreservation. NATO ASI Series (Series A: Life Sciences), Springer, Boston, MA, vol. 147, 1987.
• S. Seki and P. Mazur. Effect of warming rate on the survival of vitrified mouse oocytes and on the recrystallization of intracellular ice. Biology of reproduction. Vol. 79, No. 4, pp. 727–737, 2008.
• W. F. Rall. Factors affecting the survival of mouse embryos cryopreserved by vitrification. Cryobiology. Vol. 24, No. 5, pp.387-402, 1987.
• A. S. Teixeira, M. E. González-Benito, A. D. Molina-García. Measurement of cooling and warming rates in vitrification-based plant cryopreservation protocols. Biotechnol Prog. Vo. 30, No. 5, pp. 1177-84, 2014.
• S. Seki and P. Mazur. The dominance of warming rate over cooling rate in the survival of mouse oocytes subjected to a vitrification procedure. Cryobiology. Vol. 59, No. (1), 75–82, 2009.
• Reed, M. Barbara. Plant Cryopreservation: A Practical Guide. Springer Science & Business Media, Springer-Verlag New York Inc, 2008.
• S. Hamamah, D. Royere, J.C. Nicolle, M. Paquignon, J. Lansac. Effects of freezing- thawing on the spermatozoon nucleus: a comparative chromatin cytophotometric study in the porcine and human species. Reprod. Nutr. Dev. Vol.30, pp. 59-64, 1990.
• S. Succu, D. Bebbere, L. Bogliolo, et al. Vitrification of in vitro matured ovine oocytes affects in vitro preimplantation development and mRNA abundance. Mol. Reprod. Dev. Vol.75, pp. 538-546, 2008.
• M. Tachataki, R.M.L Winston, D.M Taylor. Quantitative RT-PCR reveals tuberous sclerosis gene, TSC2, mRNA degradation following cryopreservation in the human preimplantation embryo. Mol. Hum. Reprod. Vol. 9, pp. 593-601, 2003.
• T.C Fisher, S. Groner, U. Zentgraf, V. Hemleben. Evidence for nucleosomal phasing and a novel protein specifically binding to cucumber satellite DNA. Z. Naturforsch. Vol. 49, pp.79-86, 1994.
• S.I Peris, A. Morrier, M. Dufour, J.L Bailey. Cryopreservation of ram semen facilitates sperm DNA damage: relationship between sperm andrological parameters and the sperm chromatin structure assay. J. Androl. Vol. 25, pp. 224-233, 2004.
• J. E. Lovelock. The mechanism of the protective action of glycerol against haemolysis by freezing and thawing, Biochim. Biophys. Acta. Vol. 11, pp. 28–36, 1953.
• H. T. Meryman. The exceeding of a minimum tolerable cell volume in hypertonic suspension as a cause of freezing injury, in The Frozen Cell, Wolstenholme, G.E. and O’Connor, M., Eds., Churchill, London, pp. 51–64, 1970.
• H. T. Meryman. Freezing injury and its prevention in living cells, Annu. Rev. Biophys. Vol. 3, pp. 341–363, 1974.
• P.L. Steponkus and S.C. Wiest. Plasma membrane alterations following cold acclimation and freezing, in Plant Cold Hardiness and Freeze Stress—Mechanisms and Crop Implications, Li, P.H. and Sakai, A., Eds., Academic Press, New York, pp. 75–91, 1978.
• P. Mazur. Kinetics of water loss from cells at subzero temperatures and the likelihood of intracellular freezing, J. Gen. Physiol. Vol. 47, pp. 347–369, 1963.
• A.M.M. Zade-Oppen. Posthypertonic hemolysis in sodium chloride systems, Acta Physiol. Scand. Vol. 73, pp. 341–364, 1968.
• J. A. Elliott. Intracellular ice formation: the enigmatic role of cell-cell junctions. Biophys J. Vol. 105, No. 9, pp. 1935-1936, 2013.
• P. Mazur. The role of cell membranes in the freezing of yeast and other single cells, Ann. N.Y. Acad. Sci. Vol. 125, pp. 658–676, 1965.
• J.P. Acker and L.E. McGann. Membrane damage occurs during the formation of intracellular ice, Cryo-Letters. Vol. 22, pp. 241–254, 2001.
• W.K. Berger and B. Uhrik. Freeze-induced shrinkage of individual cells and cell-to-cell propagation of intracellular ice in cell chains from salivary glands, Experientia. Vol. 52, pp. 843–850, 1996.
• E. Asahina. Frost injury in living cells. Nature. Vol. 196, pp. 445–446, 1962.
• P.L. Steponkus, D. Stout, J. Wolfe, R. Lovelace. Freeze-induced electrical transients and cryoinjury, Cryo-Letters. Vol. 5, pp. 343–348, 1984.
• K. Muldrew and L.E. McGann. Mechanisms of intracellular ice formation, Biophys. J. Vol. 57, pp. 525–532, 1990.
• M. Toner, E.G. Cravalho, M. Karel. Thermodynamics and kinetics of intracellular ice formation during freezing of biological cells, J. Appl. Phys. Vol. 67, pp. 1582–1593, 1990.
• J.O.M. Karlsson. A theoretical model of intracellular devitrification, Cryobiology. Vol. 42, pp. 154–169, 2001.
• J. Farrant and G.J. Morris. Thermal shock and dilution shock as the causes of freezing injury, Cryobiology. Vol. 10, pp. 134–140, 1973.
• J. Farrant, C.A. Walter, H. Lee, L.E. McGann. Use of two-step cooling procedures to examine factors influencing cell survival following freezing and thawing, Cryobiology. Vol. 14, pp. 273–286, 1977.
• J. Levitt. A sulfhydryl-disulfide hypothesis of frost injury and resistance in plants, J. Theor. Biol. Vol. 3, pp. 355–391,1962.
• M.J. Ashwood-Smith, G.W Morris, R. Fowler, T.C. Appleton, R. Ashorn. Physical factors are involved in the destruction of embryos and oocytes during freezing and thawing procedures, Hum. Reprod. Vol. 3, pp.795–802, 1988.
• G.J. Morris and J.J. McGrath. Intracellular ice nucleation and gas bubble formation in spirogyra, CryoLetters. Vol. 2, pp. 341–352, 1981.
• P.L. Steponkus and M.F Dowgert. Gas bubble formation during intracellular ice formation. CryoLetters. Vol. 2, pp. 42–47, 1981.
• K. Shimada and E. Asahina. Visualization of intracellular ice crystals formed in very rapidly frozen cells at –27°C. Cryobiology. Vol. 12, pp. 209–218, 1975.
• J.C. Bischof and B. Rubinsky. Large ice crystals in the nucleus of rapidly frozen liver cells. Cryobiology. Vol. 30, pp. 597–603, 1993.
• T.H. Jang, S.C. Park, J.H. Yang, et al. Cryopreservation and its clinical applications. Integr Med Res. Vol. 6, No. 1, pp.12-18, 2017.
• H. Sieme, H. Oldenhof, W.F. Wolkers. Mode of action of cryoprotectants for sperm preservation. Anim Reprod Sci. Vol.169, pp.2-5, 2016.
• V. Berejnov, N. S. Husseini, O. A. Alsaied, R.E. Thorne. Effects of cryoprotectant concentration and cooling rate on vitrification of aqueous solutions. J. Appl. Cryst. Vol. 39, pp. 244-251, 2006.
• J. Sztein, K. Noble, J. Farley, L. Mobraaten. Comparison of Permeating and Nonpermeating Cryoprotectants for Mouse Sperm Cryopreservation. Cryobiology. Vol. 42, No. 1, pp.28-39, 2001.
• G. D. Elliott, S. Wang, B.J. Fuller. Cryoprotectants: A review of the actions and applications of cryoprotective solutes that modulate cell recovery from ultra-low temperatures. Cryobiology. Vol. 76, pp.74- 91, 2017.
• B. P. Best. Cryoprotectant Toxicity: Facts, Issues, and Questions. Rejuvenation research, 18(5), 422–436, 2015.
• S. Tsai, G. Chong, P. J. Meng, C. Lin. Sugars as supplemental cryoprotectants for marine organisms. Rev Aquacult. Vol. 10, pp. 703-715, 2018.
• J. Buitink, M.M.A.E Claessens, M.A. Hemminga, F.A Hoekstra. Influence of water content and temperature on molecular mobility and intracellular glasses in seeds and pollen, Plant Physiol. Vol. 118, pp. 531–541, 1998.
• J.H. Crowe, J.F. Carpenter, L.M. Crowe. The role of vitrification in anhydrobiosis, Annu. Rev. Physiol. Vol. 60, pp. 73–103, 1998.
• J. Wolfe, G. Bryant. Freezing, drying, and/or vitrification of membrane–solute–water systems, Cryobiology. Vol. 39, pp. 103– 129, 1999.
• B.P. Gaber, I. Chandrasekhar, N. Pattabiraman. The interaction of trehalose with the phospholipid bilayer: A molecular modeling study, in Membranes, Metabolism and Dry Organisms, Leopold, A.C., Ed., Cornell University Press, Ithaca, NY, pp. 231–241, 1986.
• J.H. Crowe, J.F. Carpenter, L.M. Crowe. Preserving dry biomaterials: The water replacement hypothesis, Part 1, Biopharm. Vol. 4, pp. 28–33, 1993.
• J.H. Crowe, J.F. Carpenter, L.M. Crowe. Preserving dry biomaterials: The water replacement hypothesis, Part 2, Biopharm. Vol. 5, pp. 40–43, 1993.
• J. M. Zhang, Y. Sheng, Y. Z Cao, H. Y Wang, Z. J Chen. Effects of cooling rates and ice-seeding temperatures on the cryopreservation of whole ovaries. Journal of assisted reproduction and genetics. Vol. 28, No.7, pp. 627–633, 2011.
• C.J. Hunt. Cryopreservation: Vitrification and Controlled Rate Cooling. Methods Mol Biol. Vol. 1590, pp.41-77, 2017. [62] S. Sukumar, S.P Kar. Numerical analysis of an enhanced cooling rate cryopreservation process in a biological tissue, Journal of Thermal Biology. Vol. 81, pp. 146-153, 2019.
• D. Gao, J. K Critser. Mechanisms of Cryoinjury in Living Cells. ILAR Journal. Vol. 41, No. 4, pp.187–196, 2000.
• S.P. Leibo, J. Farrant, P. Mazur, M.G. Hanna, L.H Smith. Effects of freezing of marrow stem cell suspensions: interaction of cooling and warming rates in the presence of PVP, sucrose and Glycerol. Cryobiology. Vol. 6, pp.315–332, 1979.
• D.G Whittingham. Some factors affecting embryo storage in laboratory animals, in: K. Elliot, J. Whelan (Eds.), The Freezing of Mammalian Embryos. Ciba Foundation 52, Elsevier, Amsterdam, pp. 97–127, 1977.
• G. Missous, B. Thammavongs, V.M. Dieuleveux, M. Guéguen, J.M Panoff. Improvement of the cryopreservation of the fungal starter Geotrichum candidum by artificial nucleation and temperature downshift control, Cryobiology. Vol. 55; pp. 66–71, 2007.
• Y. Sugawara, A. Ichi-Ishi. Application of ‘‘CryoSeeds’’ in the cryopreservation of cultured plant cells and tissues, Plant Tissue Cult. Lett. Vol. 9, pp. 47–50, 1992.
• T. Kojima, T. Soma, N. Oguri. Effect of ice nucleation by droplet of immobilized silver iodide on freezing of rabbit and bovine embryos, Theriogeneology. Vol. 30; pp. 1199–1207, 1988.
• A. Petersen, H. Schneider, G. Rau, B. Glasmacher. A new approach for freezing of aqueous solutions under active control of the nucleation temperature, Cryobiology. Vol. 53; pp. 248–257, 2006.
• P.V Hobbs. Ice Physics, Clarendon Press, Oxford, 1974.
• S. Passot, I.C. Trelea, M. Marin, M. Galen, G.J. Morris, F. Fonseca. Effects of controlled ice nuicleation on primary drying stage and protein receovery in vials cooled in a modified freeze-dryer, J. Biomech. Eng. Vol. 131; pp. 1–5, 2009.
• R. Heidemann, M. Mered, D.Q. Wang, B. Gardner, C. Zhang, J. Michaels, H. J. Henzler, N. Abbasa, K. Konstantinov. A new seed train expansion method for recombinant mammalian cell lines, Cytotechnology. Vol 38; pp 99–108, 2002.
• A.K. Konstantinidis, W. Kuu, L. Otten, S.L. Nail, R.R. Sever. Controlled nucleation in freeze drying: effects of pore size in the dried product layer, mass transfer resistance, and primary drying rate, J. Pharm. Sci. Vol 100, pp. 3453–3470, 2011.
• G.M. Fahy. The relevance of cryoprotectant "toxicity" to cryobiology. Cryobiology. Vol. 23, No. 1, pp.1-13, 1986.
• G. Verheyen, I. Pletincx, A. Van Steirteghem. Effect of freezing method, thawing temperature and post-thaw dilution/washing on motility (CASA) and morphology characteristics of high-quality human sperm. Hum Reprod. Vol. 8, No.10, pp.1678-84, 1993.
• J.O. Nöthling, R. Shuttleworth. The effect of straw size, freezing rate and thawing rate upon post-thaw quality of dog semen. Theriogenology. Vol. 15, No.5, pp.1469-80, 2005.
• Y. Sharma, M. Sharma. Sperm cryopreservation: Principles and Biology. J Infertil Reprod Biol. Vol. 8, No. 3, pp. 43- 48, 2020.
• M. Warkentin, V. Berejnov, R.E. Thorne. Hyperquenching for Protein Crystallography. J. Appl. Cryst. Vol. 39, pp. 805-811, 2006.