Skip to main content

Principles of Ice-Free Cryopreservation by Vitrification

  • Protocol
  • First Online:
Cryopreservation and Freeze-Drying Protocols

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2180))

Abstract

Vitrification is an alternative to cryopreservation by freezing that enables hydrated living cells to be cooled to cryogenic temperatures in the absence of ice. Vitrification simplifies and frequently improves cryopreservation because it eliminates mechanical injury from ice, eliminates the need to find optimal cooling and warming rates, eliminates the importance of differing optimal cooling and warming rates for cells in mixed cell type populations, eliminates the need to find a frequently imperfect compromise between solution effects injury and intracellular ice formation, and can enable chilling injury to be “outrun” by using rapid cooling without a risk of intracellular ice formation. On the other hand, vitrification requires much higher concentrations of cryoprotectants than cryopreservation by freezing, which introduces greater risks of both osmotic damage and cryoprotectant toxicity. Fortunately, a large number of remedies for the latter problem have been discovered over the past 35 years, and osmotic damage can in most cases be eliminated or adequately controlled by paying careful attention to cryoprotectant introduction and washout techniques. Vitrification therefore has the potential to enable the superior and convenient cryopreservation of a wide range of biological systems (including molecules, cells, tissues, organs, and even some whole organisms), and it is also increasingly recognized as a successful strategy for surviving harsh environmental conditions in nature. But the potential of vitrification is sometimes limited by an insufficient understanding of the complex physical and biological principles involved, and therefore a better understanding may not only help to improve present outcomes but may also point the way to new strategies that may be yet more successful in the future. This chapter accordingly describes the basic principles of vitrification and indicates the broad potential biological relevance of this alternative method of cryopreservation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Goldstein M, Simha R (1976) The Glass transition and the nature of the glassy state. In: Annals of the New York Academy of Sciences, vol 279. New York Academy of Sciences, New York

    Google Scholar 

  2. Wowk B (2010) Thermodynamic aspects of vitrification. Cryobiology 60:11–22

    Article  CAS  PubMed  Google Scholar 

  3. History of Glass. http://www.historyofglass.com/glass-history/glass-timeline/

  4. Shackley MS (2013) Archeological Obsidian Studies: Method and Theory. Adv. Archeol. Museum Sci 3:1–243

    Google Scholar 

  5. Ojovan MJ, Lee WE (2013) An Introduction to Nuclear Waste Immobilization, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  6. Hanford Vitrification Plant. http://www.bechtel.com/hanford_waste_treatment.html

  7. Luyet B (1937) The vitrification of organic colloids and of protoplasm. Biodynamica 1:1–14

    Google Scholar 

  8. Brayley EW (1860) Notes on the apparent universality of a principle analogous to regelation, on the physical nature of glass, and on the probable existence of water in a state corresponding to that of glass. Proc Roy Soc 10:450–460

    Google Scholar 

  9. Bruggeller P, Mayer E (1980) Complete vitrification in pure liquid water and dilute aqueous solutions. Nature 288:569–571

    Article  Google Scholar 

  10. Dubochet J, McDowall AW (1981) Vitrification of pure water for electron microscopy. J Microsc 124:RP3–RP4

    Article  Google Scholar 

  11. Rapatz G, Luyet B (1968) Electron microscope study of erythrocytes in rapidly cooled suspensions containing various concentrations of glycerol. Biodynamica 10:193–210

    CAS  PubMed  Google Scholar 

  12. Angell CA, Sichina W (1976) Thermodynamics of the glass transition: empirical aspects. Ann N Y Acad Sci 279:53–67

    Article  CAS  Google Scholar 

  13. Sakurai M, Furuki T, Akao K, Tanaka D, Nakahara Y, Kikawada T, Watanabe M, Okuda T (2008) Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proc Natl Acad Sci U S A 105:5093–5098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hengherr S, Worland MR, Reuner A, Brummer F, Schill RO (2009) High-temperature tolerance in anhydrobiotic tardigrades is limited by glass transition. Physiol Biochem Zool 82:749–755

    Article  CAS  PubMed  Google Scholar 

  15. Povey JF, Perez-Moral N, Noel TR, Parker R, Howard MJ, Smales CM (2009) Investigating variables and mechanisms that influence protein integrity in low water content amorphous carbohydrate matrices. Biotechnol Prog 25:1217–1227

    Article  CAS  PubMed  Google Scholar 

  16. Mensink MA, Frijlink HW, van der Voort Maarschalk K, Hinrichs WL (2017) How sugars protect proteins in the solid state and during drying (review): mechanisms of stabilization in relation to stress conditions. Eur J Pharm Biopharm 114:288–295

    Article  CAS  PubMed  Google Scholar 

  17. Fahy GM, Wowk B, Wu J (2006) Cryopreservation of complex systems: the missing link in the regenerative medicine supply chain. Rejuvenation Res 9:279–291

    Article  CAS  PubMed  Google Scholar 

  18. Fahy GM, Rall WF (2007) Vitrification: an overview. In: Liebermann J, Tucker MJ (eds) Vitrification in assisted reproduction: A user's manual and troubleshooting guide. Informa Healthcare, London, pp 1–20

    Google Scholar 

  19. Taylor MJ, Song YC, Brockbank KG (2004) Vitrification in tissue preservation: new developments. In: Fuller BJ, Lane N, Benson EE (eds) Life in the frozen state. CRC Press, Boca Raton, pp 603–641

    Chapter  Google Scholar 

  20. Fahy GM (2019) Principles of vitrification as a method of cryopreservation in reproductive biology and medicine. In: Donnez J, Kim SS (eds) Fertility preservation: principles & practice, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  21. Fahy GM, Wowk B (2015) Principles of cryopreservation by vitrification. Methods Mol Biol 1257:21–82

    Article  CAS  PubMed  Google Scholar 

  22. Fahy GM, Wowk B, Pagotan R, Chang A, Phan J, Thomson B, Phan L (2009) Physical and biological aspects of renal vitrification. Organogenesis 5:167–175

    Article  PubMed  PubMed Central  Google Scholar 

  23. Fahy GM, Wowk B, Wu J, Phan J, Rasch C, Chang A, Zendejas E (2004) Cryopreservation of organs by vitrification: perspectives and recent advances. Cryobiology 48:157–178

    Article  CAS  PubMed  Google Scholar 

  24. Luyet BJ, Gehenio PM (1939) The physical states of protoplasm at low temperatures. Review and critical study, vol 2. Biodynamica, Normandy, pp 1–128

    Google Scholar 

  25. Luyet BJ, Gehenio PM (1940) Life and death at low temperatures. Biodynamica, Normandy

    Google Scholar 

  26. MacFarlane DR (1987) Aqueous solutions: crystallization, vitrification, and liquefaction. In: Pegg DE, Karow AM Jr (eds) The biophysics of organ cryopreservation. Plenum Press, New York, pp 143–146

    Chapter  Google Scholar 

  27. Franks F, Asquith MH, Hammond CC, Skaer HB, Echlin P (1977) Polymer cryoprotectants in the preservation of biological ultrastructure. I. Low temperature states of aqueous solutions of hydrophilic polymers. J Microscopy 110:223–228

    Article  CAS  Google Scholar 

  28. Levine H, Slade L (1988) Thermomechanical properties of small-carbohydrate-water glasses and “rubbers”. J Chem Soc Faraday Trans 1 84:2619–2633

    Article  CAS  Google Scholar 

  29. Morris GJ, Goodrich M, Acton E, Fonseca F (2006) The high viscosity encountered during freezing in glycerol solutions: effects on cryopreservation. Cryobiology 52:323–334

    Article  CAS  PubMed  Google Scholar 

  30. Rasmussen DH, Luyet B (1972) Thermal analysis of "partially dehydrated" heart tissue. Biodynamica 11:149–155

    CAS  PubMed  Google Scholar 

  31. Luyet B, Rasmussen DH (1973) On some inconspicuous changes occurring in aqueous systems subjected to below zero C temperatures. Biodynamica 11:209–215

    CAS  Google Scholar 

  32. Luyet B, Rasmussen D (1967) Study by differential thermal analysis of the temperatures of instability in rapidly cooled solutions of polyvinylpyrrolidone. Biodynamica 10:137–147

    CAS  PubMed  Google Scholar 

  33. Luyet B, Rasmussen D (1968) Study by differential thermal analysis of the temperatures of instability of rapidly cooled solutions of glycerol, ethylene glycol, sucrose, and glucose. Biodynamica 10:167–191

    CAS  PubMed  Google Scholar 

  34. Rasmussen D, Luyet B (1969) Complementary study of some non-equilibrium phase transitions in frozen solutions of glycerol, ethylene glycol, glucose, and sucrose. Biodynamica 10:319–331

    Google Scholar 

  35. Rasmussen D (1969) A note about "phase diagrams" of frozen tissues. Biodynamica 10:333–339

    CAS  PubMed  Google Scholar 

  36. Knight CA (1967) The freezing of Supercooled liquids. D. Van Nostrand, Princeton

    Google Scholar 

  37. MacFarlane DR, Forsyth M, Barton CA (1991) Vitrification and devitrification in cryopreservation. In: Advances in low-temperature biology, vol 1. Elsevier, Amsterdam, pp 221–277

    Google Scholar 

  38. Mehl PM (1996) Crystallization and vitrification in aqueous glass-forming solutions. In: Advances in low-temperature biology, vol 3. Elsevier, Amsterdam, pp 185–255

    Chapter  Google Scholar 

  39. Mazur P (1966) Physical and chemical basis of injury in single-celled micro-organisms subjected to freezing and thawing. In: Meryman HT (ed) Cryobiology. Academic Press, New York, pp 214–315

    Google Scholar 

  40. Luyet BJ, Sager D, Gehenio PM (1967) The phenomenon of "premelting recrystallization". Biodynamica 10:123–132

    CAS  PubMed  Google Scholar 

  41. Boutron P, Kaufmann A (1978) Stability of the amorphous state in the system water-glycerol-dimethylsulfoxide. Cryobiology 15:93–108

    Article  CAS  PubMed  Google Scholar 

  42. Boutron P (1986) Comparison with the theory of the kinetics and extent of ice crystallization and of the glass-forming tendency in aqueous cryoprotective solutions. Cryobiology 23:88–102

    Article  CAS  PubMed  Google Scholar 

  43. Boutron P, Mehl P (1990) Theoretical prediction of devitrification tendency: determination of critical warming rates without using finite expansions. Cryobiology 27:359–377

    Article  CAS  PubMed  Google Scholar 

  44. Meryman HT (1971) Cryoprotective agents. Cryobiology 8:173–183

    Article  CAS  PubMed  Google Scholar 

  45. Karow AM Jr (1969) Cryoprotectants -- a new class of drugs. J Pharm Pharmacol 21:209–223

    Article  CAS  PubMed  Google Scholar 

  46. Fuller BJ (2004) Cryoprotectants: the essential antifreezes to protect life in the frozen state. Cryo-Letters 25:375–388

    CAS  PubMed  Google Scholar 

  47. Lovelock JE (1954) The protective action of neutral solutes against haemolysis by freezing and thawing. Biochem J 56:265–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Abazari A, Meimetis LG, Budin G, Bale SS, Weissleder R, Toner M (2015) Engineered trehalose permeable to mammalian cells. PLoS One 10:e0130323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Katkov II, Isachenko V, Isachenko E (2007) Vitrification in small quenched volumes with a minimal amount of, or without vitrificants: basic biophysics and thermodynamics. In: Tucker MJ, Liebermann J (eds) Vitrification in assisted reproduction. Informa UK, London, pp 21–32

    Chapter  Google Scholar 

  50. Wowk B, Leitl E, Rasch CM, Mesbah-Karimi N, Harris SB, Fahy GM (2000) Vitrification enhancement by synthetic ice blocking agents. Cryobiology 40:228–236

    Article  CAS  PubMed  Google Scholar 

  51. Wowk B, Fahy GM (2002) Inhibition of bacterial ice nucleation by polyglycerol polymers. Cryobiology 44:14–23

    Article  CAS  PubMed  Google Scholar 

  52. Kuwabara C, Wang D, Endoh K, Fukushi Y, Arakawa K, Fujikawa S (2013) Analysis of supercooling activity of tannin-related polyphenols. Cryobiology 67:40–49

    Article  CAS  PubMed  Google Scholar 

  53. Kuwabara C, Wang D, Kasuga J, Fukushi Y, Arakawa K, Koyama T, Inada T, Fujikawa S (2012) Freezing activities of flavonoids in solutions containing different ice nucleators. Cryobiology 64:279–285

    Article  CAS  PubMed  Google Scholar 

  54. Walters KR, Serianni AS, Sformo T, Barnes BM, Duman JG (2009) A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. Proc Natl Acad Sci U S A 106:20210–20215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Graether SP (2011) Biochemistry and Function of Antifreeze Proteins. In: Uversky VN (ed) Molecular anatomy and physiology of proteins. Nova Science Publishers, New York

    Google Scholar 

  56. Briard JG, Ferandez M, de Luna P, Woo TK, Ben RN (2016) QSAR accelerated discovery of potent ice recrystallization inhibitors. Sci Rep 6:26403. https://doi.org/10.1038/srep26403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Poisson JS, Acker JP, Briard JG, Meyer JE, Ben RN (2019) Modulating intracellular ice growth with cell permeable small molecule ice recrystallization inhibitors. Langmuir 35:7452–7458

    Article  CAS  PubMed  Google Scholar 

  58. Briard JG, Poisson JS, Turner TR, Capicciotti CJ, Acker JP, Ben RN (2016) Small molecule ice recrystallization inhibitors mitigate red blood cell lysis during freezing, transient warming and thawing. Sci Rep 6:23619. https://doi.org/10.1038/srep23619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Cao Y, Hassan M, Cheng Y, Chen Z, Wang M, Zhang X, Haider Z, Zhao G (2019) Multifunctional photo- and magnetoresponsive graphene oxide-Fe3O4 nanocomposite-alginate hydrogel platform for ice recrystallization inhibition. ACS Appl Mater Interfaces 11:12379–12388

    Article  CAS  PubMed  Google Scholar 

  60. Rall WF, Fahy GM (1985) Ice-free cryopreservation of mouse embryos at -196°C by vitrification. Nature 313:573–575

    Article  CAS  PubMed  Google Scholar 

  61. Guan N, Blomsma SA, Fahy GM, Groothuis GM, de Graaf IAM (2013) Analysis of gene expression changes to elucidate the mechanism of chilling injury in precision-cut liver slices. Toxicol In Vitro 27:890–899

    Article  CAS  PubMed  Google Scholar 

  62. McGrath JJ (1987) Cold shock: thermoelastic stress in chilled biological membranes. In: Diller KR (ed) Network Thermodynamics, Heat and Mass Transfer in Biotechnology. United Engineering Center, New York, pp 57–66

    Google Scholar 

  63. McGrath JJ, Morris GJ (1985) Cold shock injury is a significant factor in freezing injury: a position for. Cryobiology 22:628

    Article  Google Scholar 

  64. Steponkus PL, Myers SP, Lynch DV, Gardner L, Bronshteyn V, Leibo SP, Rall WF, Pitt RE, Lin TT, MacIntyre RJ (1990) Cryopreservation of Drosophila melanogaster embryos. Nature 345:170–172

    Article  CAS  PubMed  Google Scholar 

  65. Mazur P, Schneider U, Mahowald AP (1992) Characteristics and kinetics of subzero chilling injury in drosophila embryos. Cryobiology 29:39–68

    Article  CAS  PubMed  Google Scholar 

  66. Martino A, Songsasen N, Leibo SP (1996) Development into blastocysts of bovine oocytes cryopreserved by ultra-rapid cooling. Biol Reprod 54:1059–1069

    Article  CAS  PubMed  Google Scholar 

  67. Lovelock JE (1955) Haemolysis by thermal shock. Br J Haematol 1:117–129

    Article  CAS  PubMed  Google Scholar 

  68. Takahashi T, Williams RJ (1983) Thermal shock hemolysis in human red cells. I. the effects of temperature, time, and osmotic stress. Cryobiology 20:507–520

    Article  CAS  PubMed  Google Scholar 

  69. Crowe JH, Clegg JS (1973) In: Dowden (ed) Anhydrobiosis, vol 477. Hutchinson & Ross, Stroudsburg

    Google Scholar 

  70. Crowe JH, Clegg JS (1979) Dry biological systems. Academic Press, New York

    Google Scholar 

  71. Leather SR, Walters KFA, Bale JS (1993) The ecology of insect overwintering. Cambridge University Press, Cambridge (UK)

    Book  Google Scholar 

  72. Lee RE Jr, Denlinger DL (1991) Insects at low temperature. Chapman and Hall, New York

    Book  Google Scholar 

  73. Crowe JH, Crowe LM, Tablin F, Wolkers W, Oliver AE, Tsvetkova NM (2004) Stabilization of cells during freeze-drying: the trehalose myth. In: Fuller BJ, Lane N, Benson EE (eds) Life in the Frozen State. CRC Press, Boca Raton, pp 581–601

    Chapter  Google Scholar 

  74. Acker JP, Chen T, Fowler A, Toner M (2004) Engineering desiccation tolerance in mammalian cells: tools and techniques. In: Fuller BJ, Lane N, Benson EE (eds) Life in the Frozen State. CRC Press, Boca Raton, pp 563–580

    Chapter  Google Scholar 

  75. Levitt J (1965) Thiogel -- a model system for demonstrating intermolecular disulfide bond formation on freezing. Cryobiology 1:312–316

    Article  CAS  PubMed  Google Scholar 

  76. Morton WM (1969) Effects of freezing and hardening on the sulfhydryl groups of protein fractions from cabbage leaves. Plant Physiol 44:168–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ishiwata S (1976) Freezing of actin. Reversible oxidation of a sulfhydryl group and structural change. J Biochem 80:595–609

    Article  CAS  PubMed  Google Scholar 

  78. Takahashi T, Asahina E (1977) Protein-bound SH groups in frozen-thawed egg cells of the sea urchin. Cryobiology 14:367–372

    Article  CAS  PubMed  Google Scholar 

  79. Chatterjee S, de Lamirande E, Gagnon C (2001) Cryopreservation alters membrane sulfhydryl status of bull spermatozoa: protection by oxidized glutathione. Mol Reprod Dev 60:498–506

    Article  CAS  PubMed  Google Scholar 

  80. Tappel AL (1966) Effects of low temperatures and freezing on enzymes and enzyme systems. In: Meryman HT (ed) Cryobiology. Academic Press, New York, pp 163–177

    Google Scholar 

  81. Lone SA, Mohanty TK, Baithalu RK, Yadav HP (2019) Sperm protein carbonylation. Andrologia 51:e13233

    Article  PubMed  CAS  Google Scholar 

  82. Crowe JH, Hoekstra FA, Crowe LM, Anchordoguy TJ, Drobnis E (1989) Lipid phase transitions measured in intact cells with Fourier transform infrared spectroscopy. Cryobiology 26:78–84

    Article  Google Scholar 

  83. Zeron Y, Tomczak M, Crowe J, Arav A (2002) The effect of liposomes on thermotropic membrane phase transitions of bovine spermatozoa and oocytes: implications for reducing chilling sensitivity. Cryobiology 45:143–152

    Article  CAS  PubMed  Google Scholar 

  84. Wolkers WF, Oldenhof H, Tang F, Han J, Bigalk J, Sieme H (2019) Factors affecting the membrane permeability barrier function of cells during preservation technologies. Langmuir 35:7520–7528

    Article  CAS  PubMed  Google Scholar 

  85. Webb MS, Hui SW, Steponkus PL (1993) Dehydration-induced lamellar-to-hexagonal-II phase transitions in DOPE/DOPC mixtures. Biochim Biophys Acta 1145:93–104

    Article  CAS  PubMed  Google Scholar 

  86. Steponkus PL, Wolfe J, Dowgert MF (1981) Stresses induced by contraction and expansion during a freeze-thaw cycle: a membrane perspective. In: Morris GJ, Clarke A (eds) Effects of Low Temperatures on Biological Membranes. Academic Press, New York, pp 307–322

    Google Scholar 

  87. Fahy GM (1988) Vitrification. In: McGrath JJ, Diller KR (eds) Low temperature biotechnology: emerging applications and engineering contributions. American society of Mechanical Engineers, New York, pp 113–146

    Google Scholar 

  88. Fahy GM (1990) Vitrification as an approach to organ cryopreservation: past, present, and future. In: Sibinga CTS, Das PC, Meryman HT (eds) Cryopreservation and low temperature biology in blood transfusion. Kluwer, Boston, pp 255–268

    Chapter  Google Scholar 

  89. Mullen SF, Fahy GM (2011) Fundamental aspects of vitrification as a method of reproductive cell, tissue, and organ cryopreservation. In: Donnez J, Kim S (eds) Principles & Practice of Fertility Preservation. Cambridge University Press, Cambridge, pp 145–163

    Chapter  Google Scholar 

  90. Stiles W (1930) On the cause of cold death of plants. Protoplasma 9:459–468

    Article  Google Scholar 

  91. Tammann G (1898) Ueber die Abhangigkeit der Zahl der Kerne, welche sich in verschiedenen unterkuhlten Flussigkeiten bilden, vom der temperatur. Z Phys Chem 25:441–479

    Article  CAS  Google Scholar 

  92. Moran T (1926) The freezing of gelatin gel. Proc Roy Soc A 112:30–46

    CAS  Google Scholar 

  93. Hardy WB (1926) A microscopic study of the freezing of gel. Proc Roy Soc A 112:47–61

    CAS  Google Scholar 

  94. Anonymous (1975) Curriculum vitae and list of publications of B. J. Luyet. Cryobiology 12:440–453

    Google Scholar 

  95. Goetz A, Goetz SS (1938) Death by devitrification in yeast cells. Biodynamica 2:1–8

    Google Scholar 

  96. Goetz A, Goetz SS (1938) Vitrification and crystallization of organic cells at low temperatures. J Appl Phys 9:718–729

    Article  CAS  Google Scholar 

  97. Luyet BJ, Thoennes G (1938) The survival of plant cells immersed in liquid air. Science 88:284–285

    Article  CAS  PubMed  Google Scholar 

  98. Smith AU (1954) Effects of low temperatures on living cells and tissues. In: Harris RJC (ed) Biological applications of freezing and drying. Academic Press, New York, pp 1–53

    Google Scholar 

  99. Luyet BJ, Gehenio PM (1954) Effect of the rewarming velocity on the survival of embryonic tissues frozen after treatment with ethylene glycol. Biodynamica 7:213–223

    CAS  PubMed  Google Scholar 

  100. Luyet B, Rapatz G (1958) Patterns of ice formation in some aqueous solutions. Biodynamica 8:1–68

    CAS  Google Scholar 

  101. Meryman HT (1958) X-ray analysis of rapidly frozen gelatin gels. Biodynamica 8:69–72

    CAS  Google Scholar 

  102. Luyet B (1969) On the amount of water remaining amorphous in frozen aqueous solutions. Biodynamica 10:277–291

    Google Scholar 

  103. Farrant J (1965) Mechanism of cell damage during freezing and thawing and its prevention. Nature 205:1284–1287

    Article  CAS  Google Scholar 

  104. Pegg DE, Wang L, Vaughan D (2006) Cryopreservation of articular cartilage. Part 3: the liquidus tracking method. Cryobiology 52:360–368

    Article  CAS  PubMed  Google Scholar 

  105. Fahy GM, MacFarlane DR, Angell CA, Meryman HT (1984) Vitrification as an approach to cryopreservation. Cryobiology 21:407–426

    Article  CAS  PubMed  Google Scholar 

  106. Kemp E, Clark PB, Anderson CK, Parsons FM (1966) Long-term preservation of the kidney. Proc Eur Dial Transplant Assoc 3:236–240

    Google Scholar 

  107. Luyet BJ (1966) Anatomy of the freezing process in physical systems. In: Meryman HT (ed) Cryobiology. Academic Press, New York, pp 115–138

    Google Scholar 

  108. Kroener C, Luyet B (1966) Discontinuous change in expansion coefficient at the glass transition temperature in aqueous solutions of glycerol. Biodynamica 10:41–45

    CAS  PubMed  Google Scholar 

  109. Kroener C, Luyet B (1966) Formation of cracks during the vitrification of glycerol solutions and disappearance of the cracks during rewarming. Biodynamica 10:47–52

    CAS  PubMed  Google Scholar 

  110. Rasmussen D, Luyet B (1970) Contribution to the establishment of the temperature-concentration curves of homogeneous nucleation in solutions of some cryoprotective agents. Biodynamica 11:33–44

    CAS  PubMed  Google Scholar 

  111. Luyet B, Kroener C (1966) The temperature of the "glass transition" in aqueous solutions of glycerol and ethylene glycol. Biodynamica 10:33–40

    CAS  PubMed  Google Scholar 

  112. Choremis C, Economou-Mavrou C, Tsenghi C (1961) Sodium, potassium, water, and haemoglobin in the packed red cells of severe thalassaemia. J Clin Pathol 14:637–643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Gonzales F, Luyet B (1950) Resumption of heart beat in chick embryo frozen in liquid nitrogen. Biodynamica 7:1–5

    CAS  PubMed  Google Scholar 

  114. Luyet BJ, Gonzales F (1953) Growth of nerve tissue after freezing in liquid nitrogen. Biodynamica 7:171–174

    CAS  PubMed  Google Scholar 

  115. Luyet B, Hodapp A (1938) Revival of frog's spermatozoa vitrified in liquid air. Proc Meet Soc Exp Biol 39:443–434

    Google Scholar 

  116. Rapatz G (1970) Resumption of activity in frog hearts after exposure to very low temperatures. Cryobiology 6:588

    Article  Google Scholar 

  117. Rapatz G (1972) Recovery of activity of frog hearts after exposure to −78 °C. Cryobiology 9:322

    Google Scholar 

  118. Rapatz G, Keener R (1974) Effect of concentration of ethylene glycol on the recovery of frog hearts after freezing to low temperatures. Cryobiology 11:571–572

    Article  Google Scholar 

  119. Elford BC (1970) Functional recovery of smooth muscle after exposure to dimethyl sulfoxide and low temperatures. Cryobiology 7:148–153

    Article  CAS  PubMed  Google Scholar 

  120. Elford BC, Walter CA (1972) Effects of electrolyte composition and pH on the structure and function of smooth muscle cooled to −79 °C in unfrozen media. Cryobiology 9:82–100

    Article  CAS  PubMed  Google Scholar 

  121. Boutron P, Alben R (1975) Structural model for amorphous solid water. J Chem Phys 62:4848–4853

    Article  CAS  Google Scholar 

  122. Boutron P, Kaufmann A (1978) Metastable states in the system water-ethanol. Existence of a second hydrate, curious properties of both hydrates. J Chem Phys 68:5032–5041

    Article  CAS  Google Scholar 

  123. Boutron P, Kaufmann A (1979) Stability of the amorphous state in the system water-glycerol-ethylene glycol. Cryobiology 16:83–89

    Article  CAS  PubMed  Google Scholar 

  124. Boutron P, Kaufmann A (1979) Maximum in the stability of the amorphous state in the system water-glycerol-ethanol. Cryobiology 16:372–389

    Article  CAS  PubMed  Google Scholar 

  125. Boutron P (1979) Stability of the amorphous state in the system water-1,2-propanediol. Cryobiology 16:557–568

    Article  CAS  PubMed  Google Scholar 

  126. James ER, Farrant J (1977) Recovery of infective Schistosoma mansoni schistosomula from liquid nitrogen: a step towards storage of a live schistosomiasis vaccine. Trans Roy Soc Trop Med Hyg 71:498–500

    Article  CAS  PubMed  Google Scholar 

  127. James ER (1980) Cryopreservation of Schistosoma mansoni schistosomula using 40% v/v (10M) methanol and rapid cooling. Cryo-Letters 1:535–544

    Google Scholar 

  128. Fahy GM (1977) Correlations between cryoinjury in mammalian systems and changes in the composition and properties of the extracellular milieu during freezing. In: Department of Pharmacology. Medical College of Georgia, Augusta, p 302

    Google Scholar 

  129. Fahy GM (1981) Prospects for vitrification of whole organs. Cryobiology 18:617

    Article  Google Scholar 

  130. Fahy GM (1981) Analysis of "solution effects" injury: cooling rate dependence of the functional and morphological sequellae of freezing in rabbit renal cortex protected with dimethyl sulfoxide. Cryobiology 18:550–570

    Article  CAS  PubMed  Google Scholar 

  131. MacFarlane DR, Angell CA, Fahy GM (1981) Homogeneous nucleation and glass formation in cryoprotective systems at high pressures. Cryo-Letters 2:353–358

    CAS  Google Scholar 

  132. Fahy GM, MacFarlane DR, Angell CA (1982) Recent progress toward vitrification of kidneys. Cryobiology 19:668–669

    Article  Google Scholar 

  133. Fahy GM, Hirsh A (1982) Prospects for organ preservation by vitrification. In: Pegg DE, Jacobsen IA, Halasz NA (eds) Organ preservation, basic and applied aspects. MTP Press, Lancaster, pp 399–404

    Chapter  Google Scholar 

  134. Fahy GM, MacFarlane DR, Angell CA, Meryman HT (1983) Vitrification as an approach to cryopreservation. Cryobiology 20:699

    Google Scholar 

  135. Fahy GM (1982) Prevention of toxicity from high concentrations of cryoprotective agents. In: Pegg DE, Jacobsen IA, Halasz NA (eds) Organ preservation, basic and applied aspects. MTP Press, Lancaster, pp 367–369

    Chapter  Google Scholar 

  136. Fahy GM (1983) Cryoprotectant toxicity neutralizers reduce freezing damage. Cryo-Letters 4:309–314

    CAS  Google Scholar 

  137. Fahy GM (1984) Cryoprotectant toxicity: biochemical or osmotic? Cryo-Letters 5:79–90

    CAS  Google Scholar 

  138. Fahy GM (1984) Cryoprotectant toxicity reduction: specific or nonspecific? Cryo-Letters 5:287–294

    CAS  Google Scholar 

  139. Rall WF, Reid DS, Farrant J (1980) Innocuous biological freezing during warming. Nature 286:511–514

    Article  CAS  PubMed  Google Scholar 

  140. Rall WF (1981) The role of intracellular ice in the slow warming injury of mouse embryos. In: Zeilmaker GH (ed) Frozen Storage of Laboratory Animals. Gustav Fischer Verlag, New York, pp 33–44

    Google Scholar 

  141. Lehn-Jensen H, Rall WF (1983) Cryomicroscopic observations of cattle embryos during freezing and thawing. Theriogenology 19:263–277

    Article  CAS  PubMed  Google Scholar 

  142. Takahashi T, Hirsh A, Erbe EF, Bross JB, Steere RL, Williams RJ (1986) Vitrification of human monocytes. Cryobiology 23:103–115

    Article  CAS  PubMed  Google Scholar 

  143. Sakai A, Kobayashi S, Oiyama I (1990) Cryopreservation of nucellar cells of navel orange (Citrus sinensis Osb. Va. Brasiliensis Tanaka) by vitrification. Plant Cell Rep 9:30–33

    Article  CAS  PubMed  Google Scholar 

  144. Sakai A (2004) Plant cryopreservation. In: Fuller BJ, Lane N, Benson EE (eds) Life in the frozen state. CRC Press, Boca Raton, pp 329–345

    Chapter  Google Scholar 

  145. Mazur P, Cole KW, Hall JW, Schreuders PD, Mahowald AP (1992) Cryobiological preservation of drosophila embryos. Science 258:1896–1897

    Article  Google Scholar 

  146. Vajta G, Kuwayama M, Vanderzwalmen P (2007) Disadvantages and benefits of vitrification. In: Tucker MJ, Liebermann J (eds) Vitrification in Assisted Reproduction, A User's Manual and Trouble-Shooting Guide. Informa UK, London, pp 33–44

    Chapter  Google Scholar 

  147. Song YC, Khirabadi BS, Lightfoot F, Brockbank KG, Taylor MJ (2000) Vitreous cryopreservation maintains the function of vascular grafts. Nat Biotechnol 18:296–299

    Article  CAS  PubMed  Google Scholar 

  148. Kheirabadi B, Fahy GM (2000) Permanent life support by kidneys perfused with a vitrifiable (7.5 molar) cryoprotectant solution. Transplantation 70:51–57

    CAS  PubMed  Google Scholar 

  149. Lovelock JE (1953) The mechanism of the protective action of glycerol against haemolysis by freezing and thawing. Biochim Biophys Acta 11:28–36

    Article  CAS  PubMed  Google Scholar 

  150. Kylin H (1917) Uber die Kalteresistenze der Meeresalgen. Ber desch bot Ges 35:370–384

    Google Scholar 

  151. Muller-Thurgau H (1886) Uber das Gefrieren and Erfrieren der Pflanzen. II Theil. Landw Jahrb (Berlin) 15:453–610

    Google Scholar 

  152. Chambers R, Hale HP (1932) The formation of ice in protoplasm. Proc Roy Soc Ser B 110:336–352

    CAS  Google Scholar 

  153. Meryman HT (1970) The exceeding of a minimum tolerable cell volume in hypertonic suspension as a cause of freezing injury. In: Wolstenholme GEW, O'Connor M (eds) The frozen cell. J & A Churchill, London, pp 51–64

    Google Scholar 

  154. Meryman HT (1968) Modified model for the mechanism of freezing injury in erythrocytes. Nature 218:333–336

    Article  CAS  PubMed  Google Scholar 

  155. Meryman HT (1971) Osmotic stress as a mechanism of freezing injury. Cryobiology 8:489–500

    Article  CAS  PubMed  Google Scholar 

  156. Meryman HT (1974) Freezing injury and its prevention in living cells. Annu Rev Biophys Bioeng 3:341–363

    Article  CAS  PubMed  Google Scholar 

  157. Mazur P (1963) Kinetics of water loss from cells at subzero temperatures and the likelihood of intracellular freezing. J Gen Physiol 47:347–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Mazur P (1970) Cryobiology: the freezing of biological systems. Science 168:939–949

    Article  CAS  PubMed  Google Scholar 

  159. Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Physiol 247:C125–C142

    Article  CAS  PubMed  Google Scholar 

  160. Mazur P (1988) Stopping biological time. The freezing of living cells. Ann N Y Acad Sci 541:514–531

    Article  CAS  PubMed  Google Scholar 

  161. Mazur P (2004) Principles of cryobiology. In: Fuller BJ, Lane N, Benson EE (eds) Life in the Frozen State. CRC Press, Boca Raton, pp 3–65

    Chapter  Google Scholar 

  162. Mazur P, Leibo SP, Farrant J, Chu EHY, Hanna MG, Smith LH (1970) Interactions of cooling rate, warming rate and protective additive on the survival of frozen mammalian cells. In: Wolstenholme GEW, O'Connor M (eds) The Frozen Cell. J&A Churchill, London, pp 69–85

    Google Scholar 

  163. Fahy GM, Karow AM Jr (1977) Ultrastructure-function correlative studies for cardiac cryopreservation. V. Absence of a correlation between electrolyte toxicity and cryoinjury in the slowly frozen, cryoprotected rat heart. Cryobiology 14:418–427

    Article  CAS  PubMed  Google Scholar 

  164. Fahy GM (1986) The relevance of cryoprotectant "toxicity" to cryobiology. Cryobiology 23:1–13

    Article  CAS  PubMed  Google Scholar 

  165. Meryman HT, Williams RJ, Douglas MSJ (1977) Freezing injury from "solution effects" and its prevention by natural or artificial cryoprotection. Cryobiology 14:287–302

    Article  CAS  PubMed  Google Scholar 

  166. Fahy GM (1986) Vitrification: a new approach to organ cryopreservation. Prog Clin Biol Res 224:305–335

    CAS  PubMed  Google Scholar 

  167. Berthelot F, Martinat-Botte F, Perreau C (2001) Birth of piglets after OPS vitrification and transfer of compacted morula stage embryos with intact zona pellucida. Reprod Nutr Dev 41:267–272

    Article  CAS  PubMed  Google Scholar 

  168. Pollack GA, Pegg DE, Hardie IR (1986) An isolated perfused rat mesentery model for direct observation of the vasculature during cryopreservation. Cryobiology 23:500–511

    Article  Google Scholar 

  169. Taylor MJ, Pegg DE (1983) The effect of ice formation on the function of smooth muscle tissue stored at −21 or −60°C. Cryobiology 20:36–40

    Article  CAS  PubMed  Google Scholar 

  170. Pegg, D.E., Diaper, M.P. The mechanism of cryoinjury in glycerol-treated rabbit kidneys, in Organ preservation, basic and applied aspects, D.E. Pegg, I.A. Jacobsen, and N.A. Halasz, Editors. 1982, MTP Press, Ltd: Lancaster. p. 389-393

    Google Scholar 

  171. Hunt CJ (1984) Studies on cellular structure and ice location in frozen organs and tissues: the use of freeze-substitution and related techniques. Cryobiology 21:385–402

    Article  CAS  PubMed  Google Scholar 

  172. Pegg DE (1987) Ice crystals in tissues and organs. In: Pegg DE, Karow AM Jr (eds) The Biophysics of Organ Cryopreservation. Plenum, New York, pp 117–140

    Chapter  Google Scholar 

  173. Pegg DE (2010) The relevance of ice crystal formation for the cryopreservation of tissues and organs. Cryobiology 60:S36–S44

    Article  PubMed  Google Scholar 

  174. Taylor MJ (1984) Sub-zero preservation and the prospect of long-term storage of multicellular tissues and organs. In: Calne RY (ed) Transplantation Immunology: Clinical and experimental. Oxford University Press, Oxford, pp 360–390

    Google Scholar 

  175. Hunt CJ, Taylor MJ, Pegg DE (1982) Freeze-substitution and isothermal freeze fixation studies to elucidate the pattern of ice formation on smooth muscle at 252K (−21 °C). J Microsc 125:177–186

    Article  CAS  PubMed  Google Scholar 

  176. Jacobsen IA, Pegg DE, Starklint H, Chemnitz J, Hunt C, Barfort P, Diaper MP (1984) Effect of cooling and warming rate on glycerolized rabbit kidneys. Cryobiology 21:637–653

    Article  CAS  PubMed  Google Scholar 

  177. Pegg DE, Jacobsen IA, Armitage WJ, Taylor MJ (1979) Mechanisms of cryoinjury in organs. In: Pegg DE, Jacobsen IA (eds) Organ Preservation II. Churchill Livingstone, New York, pp 132–144

    Google Scholar 

  178. Brockbank KGM, Taylor MJ (2007) Tissue preservation. In: Baust JG, Baust JM (eds) Advances in Biopreservation. Taylor & Francis Group, Boca Raton, pp 157–196

    Google Scholar 

  179. Fahy GM, Takahashi T, Meryman HT (1986) Practical aspects of ice-free cryopreservation. In: Sibinga CTS, Das PC, Greenwalt TJ (eds) Future Developments in Blood Banking. Martinus Nijhoff Publishing, Boston, pp 111–122

    Chapter  Google Scholar 

  180. Fahy GM, Saur J, Williams RJ (1990) Physical problems with the vitrification of large biological systems. Cryobiology 27:492–510

    Article  CAS  PubMed  Google Scholar 

  181. Rall WF, Meyer TK (1989) Zona fracture damage and its avoidance during the cryopreservation of mammalian embryos. Theriogenology 31:683–692

    Article  CAS  PubMed  Google Scholar 

  182. Williams RJ, Carnahan DL (1990) Fracture faces and other interfaces as ice nucleation sites. Cryobiology 27:479–482

    Article  CAS  PubMed  Google Scholar 

  183. Schiewe MC, Zozula S, Anderson RE, Fahy GM (2015) Validation of microSecure vitrification (uS-VTF) for the effective cryopreservation of human embryos and oocytes. Cryobiology 71:264–272

    Article  PubMed  Google Scholar 

  184. Nickell PK, Sass S, Verleve D, Blumenthal EM, Duman JG (2013) Antifreeze proteins in the primary urine of larvae of the beetle Dendroides canadensis. J Exp Biol 216:1695–1703

    CAS  PubMed  Google Scholar 

  185. Sformo T, Walters K, Jeannet K, Wowk B, Fahy G, Barnes BM, Duman JG (2010) Deep supercooling, vitrification and limited survival to -100oC in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae). J Exp Biol 213:502–509

    Article  CAS  PubMed  Google Scholar 

  186. Cosman, B. (2013) This is the new coldest temperature ever recorded on earth

    Google Scholar 

  187. Elster J, Benson EE (2004) Life in the polar terrestrial environment with a focus on algae and cyanobacteria. In: Fuller BJ, Lane N, Benson EE (eds) Life in the frozen state. CRC Press, Boca Raton, pp 111–150

    Chapter  Google Scholar 

  188. Scambos TA, Campbell GG, Pope A, Haran T, Muto A, Lazzara M, Reijmer CH, van den Broeke MR (2018) Ultralow surface temperatures in East Antarctica from satellite thermal infrared mapping: The coldest places on earth. Geophys Res Lett 45:6124–6133. https://doi.org/10.1029/2018GL078133

    Article  Google Scholar 

  189. Bennett VA, Sformo T, Walters K, Toien O, Jeannet K, Hochstrasser R, Pan Q, Serianni AS, Barnes BM, Duman JG (2005) Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): roles of antifreeze proteins, polyols, dehydration and diapause. J Exp Biol 208(Pt 23):4467–4477

    Article  CAS  PubMed  Google Scholar 

  190. Sun WQ, Leopold AC (1997) Cytoplasmic vitrification and survival of anhydrobiotic organisms. Comp Biochem Physiol 117A:327–333

    Article  CAS  Google Scholar 

  191. Burke MJ (1986) The glassy state and survival of anhydrous biological systems. In: Leopold AC (ed) Membranes, Metabolism, and Dry Organisms. Cornell University Press, Ithaca, pp 358–364

    Google Scholar 

  192. Holmstrup M, Bayley M, Ramlov H (2002) Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates. Proc Natl Acad Sci 99:5716–5720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Crowe JH, Jackson S, Crowe LM (1983) Nonfreezable water in anhydrobiotic nematodes. Mol Physiol 3:99–105

    Google Scholar 

  194. Buitink J, Leprince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215–228

    Article  CAS  PubMed  Google Scholar 

  195. Hirsh AG, Williams RJ, Meryman HT (1985) A novel method of natural cryoprotection: intracellular glass formation in deeply frozen populus. Plant Physiol 79:41–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Rall WF, Reid DS, Polge C (1984) Analysis of slow-warming injury of mouse embryos by cryomicroscopical and physicochemical methods. Cryobiology 21:106–121

    Article  CAS  PubMed  Google Scholar 

  197. Ediger MD, Angell CA, Nagel SR (1996) Supercooled liquids and glasses. J Phys Chem 100:13200–13212

    Article  CAS  Google Scholar 

  198. Kauzmann W (1948) The nature of the glassy state and the behavior of liquids at low temperatures. Chem Rev 43:219–256

    Article  CAS  Google Scholar 

  199. Forsyth M, MacFarlane DR (1986) Recrystallization revisited. Cryo-Letters 7:367–378

    CAS  Google Scholar 

  200. Mazur P, Seki S (2011) Survival of mouse oocytes after being cooled in a vitrification solution to -196°C at 95o to 70,000 °C min and warmed at 610o to 118,000 °C/min: a new paradigm for cryopreservation by vitrification. Cryobiology 62:1–7

    Article  CAS  PubMed  Google Scholar 

  201. Boutron P, Arnaud F (1984) Comparison of the cryoprotection of red blood cells by 1,2-propanediol and glycerol. Cryobiology 21:348–358

    Article  CAS  PubMed  Google Scholar 

  202. Rall WF (1987) Factors affecting the survival of mouse embryos cryopreserved by vitrification. Cryobiology 24:387–402

    Article  CAS  PubMed  Google Scholar 

  203. Dorsey NE (1948) The freezing of Supercooled water. Trans Am Philos Soc 38:247–328

    Article  CAS  Google Scholar 

  204. Jackson CL, McKenna GB (1990) The melting behavior of organic materials confined in porous solids. J Chem Phys 93:9002–9011

    Article  CAS  Google Scholar 

  205. Angell CA (1982) Supercooled water. In: Franks F (ed) Water, A Comprehensive Treatise. Plenum, New York, pp 1–81

    Google Scholar 

  206. Rasmussen DH, MacCaulay MN, MacKenzie AP (1975) Supercooling and nucleation of ice in single cells. Cryobiology 12:328–339

    Article  CAS  PubMed  Google Scholar 

  207. Franks F (1982) The properties of aqueous solutions at subzero temperatures. In: Franks F (ed) Water, a comprehensive treatise. Plenum, New York, pp 215–338

    Google Scholar 

  208. Pruppacher HR, Klett JD (1996) Homogeneous nucleation. In: Pruppacher HR, Klett JD (eds) Microphysics of Clouds and Precipitation, Second revised and expanded edition with an introduction to cloud chemistry and cloud electricity. Springer, Dordrecht Heidelberg London New York, pp 191–215

    Google Scholar 

  209. Pruppacher HR, Klett JD (1996) Heterogeneous nucleation. In: Pruppacher HR, Klett JD (eds) Microphysics of clouds and precipitation, second revised and expanded edition with an introduction to cloud chemistry and cloud electricity. Springer, Dordrecht Heidelberg London New York, pp 287–360

    Google Scholar 

  210. Maki LR, Galyan EL, Chang-Chien MM, Caldwell DR (1974) Ice nucleation induced by pseudomonas syringae. Appl Environ Microbiol 28:456–459

    Article  CAS  Google Scholar 

  211. Gavish M, Popovitz-Biro R, Lahav M, Leiserowitz L (1990) Ice nucleation by alcohols arranged in monolayers at the surface of water drops. Science 250:973–975

    Article  CAS  PubMed  Google Scholar 

  212. Earle ME, Kuhn T, Khalizov AF, Sloan JJ (2010) Volume nucleation rates for homogeneous freezing in supercooled water microdroplets: results from a combined experimental and modelling approach. Atmos Chem Phys 10:7945–7961

    Article  CAS  Google Scholar 

  213. Dupuy J, Jal JF, Ferradou C, Chieux P, Wright AF, Calemczuk R, Angell CA (1982) Controlled nucleation and quasi-ordered growth of ice crystals from low temperature electrolyte solutions. Nature 296:135–140

    Article  Google Scholar 

  214. Angell CA, Sare EJ, Donnella J, MacFarlane DR (1981) Homogeneous nucleation and glass transition temperatures in solutions of lithium salts in water-D2 and water. Doubly unstable glass regions. J Phys Chem 85:1461–1464

    Article  CAS  Google Scholar 

  215. Fahy GM (1998) Fundamentals of vitrification: tissues and organs. Cryobiology 37:380–381

    Google Scholar 

  216. Wowk B (2013) Metastable vitrification of cryoprotectant solutions. Cryobiology 67:409

    Article  Google Scholar 

  217. Mehl P (1993) Nucleation and crystal growth in a vitrification solution tested for organ cryopreservation by vitrification. Cryobiology 30:509–518

    Article  CAS  PubMed  Google Scholar 

  218. Wowk B, Fahy GM (2007) Ice nucleation and growth in concentrated vitrification solutions. Cryobiology 55:330

    Article  Google Scholar 

  219. Fahy GM (2015) Understanding and controlling ice nucleation and growth in the renal inner medulla. Cryobiology 71:540

    Article  Google Scholar 

  220. Boutron P (1993) Glass-forming tendency and stability of the amorphous state in solutions of a 2,3-butanediol containing mainly the levo and dextro isomers in water, buffer, and euro-Collins. Cryobiology 30:86–97

    Article  CAS  Google Scholar 

  221. Wowk B, Fahy GM, Ahmedyar S, Taylor MJ, Rabin Y (2018) Vitrification tendency and stability of DP6-based vitrification solutions for complex tissue cryopreservation. Cryobiology 82:70–77. https://doi.org/10.1016/j.cryobiol.2018.04.0006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  222. Baudot A, Alger L, Boutron P (2000) Glass-forming tendency in the system water-dimethyl sulfoxide. Cryobiology 40:151–158

    Article  CAS  PubMed  Google Scholar 

  223. Vigier G, Vassoille R (1987) Ice nucleation and crystallization in water-glycerol mixtures. Cryobiology 24:345–354

    Article  CAS  Google Scholar 

  224. Luyet B (1967) On the possible biological significance of some physical changes encountered in the cooling and the rewarming of aqueous solutions. In: Asahina E (ed) Cellular injury and resistance in freezing organisms. Hokkaido University, Sapporo, pp 1–20

    Google Scholar 

  225. Baudot A, Odagescu V (2004) Thermal properties of ethylene glycol and aqueous solutions. Cryobiology 48:283–294

    Article  CAS  PubMed  Google Scholar 

  226. Fahy GM (1987) Biological effects of vitrification and devitrification. In: Pegg DE, Karow AM Jr (eds) The biophysics of organ cryopreservation. Plenum Press, New York, pp 265–293

    Chapter  Google Scholar 

  227. Fahy GM, Levy DI, Ali SE (1987) Some emerging principles underlying the physical properties, biological actions, and utility of vitrification solutions. Cryobiology 24:196–213

    Article  CAS  PubMed  Google Scholar 

  228. Fahy GM (2015) Overview of biological vitrification. In: Liebermann J, Tucker M (eds) Vitrification in assisted reproduction: from basic science to clinical application. Taylor & Francis books, Ltd, New York, pp 1–22

    Google Scholar 

  229. MacFarlane DR (1986) Devitrification in glass-forming aqueous solutions. Cryobiology 23:230–244

    Article  CAS  Google Scholar 

  230. MacFarlane DR, Forsyth M (1987) Devitrification and recrystallization of glass forming aqueous solutions. In: Pegg DE, Karow AM Jr (eds) The biophysics of organ cryopreservation. Plenum Press, New York, pp 237–257

    Chapter  Google Scholar 

  231. Mehl P, Boutron P (1988) Cryoprotection of red blood cells by 1,3-butanediol and 2,3-butanediol. Cryobiology 25:44–54

    Article  CAS  PubMed  Google Scholar 

  232. Seki S, Jin B, Mazur P (2014) 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

    Article  PubMed  Google Scholar 

  233. Fahy GM (1995) The role of nucleation in cryopreservation. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, St. Paul, pp 315–336

    Google Scholar 

  234. Baudot A, Peyridieu JF, Boutron P, Mazuer J, Odin J (1996) Effects of saccharides on the glass-forming tendency and stability of solutions of 2,3-butanediol, 1,2-propanediol, or 1,3-butanediol in water, phosphate-buffered saline, euro-Collins solution, or Saint Thomas cardioplegic solution. Cryobiology 33:363–375

    Article  CAS  PubMed  Google Scholar 

  235. Wowk B, Fahy GM (2005) Toward large organ vitrification: extremely low critical cooling and warming rates of M22 vitrification solution. Cryobiology 51:362

    Google Scholar 

  236. Fahy G (2013) Consequences and control of ice formation in the renal inner medulla. Cryobiology 67:409–410

    Article  Google Scholar 

  237. Wusteman M, Robinson M, Pegg D (2004) Vitrification of large tissues with dielectric warming: biological problems and some approaches to their solution. Cryobiology 48:284–294

    Article  CAS  Google Scholar 

  238. Ruggera PS, Fahy GM (1990) Rapid and uniform electromagnetic heating of aqueous cryoprotectant solutions from cryogenic temperatures. Cryobiology 27:465–478

    Article  CAS  PubMed  Google Scholar 

  239. Burdette EC, Wiggins S, Brown R, Karow AM Jr (1980) Microwave thawing of frozen kidneys: a theoretically based experimentally-effective design. Cryobiology 17:393–402

    Article  CAS  PubMed  Google Scholar 

  240. Wowk B (2013) Adaptation of a commercial diathermy machine for radiofrequency warming of vitrified organs. Cryobiology 67:404

    Article  Google Scholar 

  241. Etheridge ML, Xu Y, Choi J, Bischof JC (2013) Radiofrequency heating of magnetic nanoparticle cryoprotectant solutions for improved cryopreservation protocols. Cryobiology 67:398–399

    Article  Google Scholar 

  242. Inada T, Lu S (2003) Inhibition of recrystallization of ice grains by adsorption of poly(vinyl alcohol) onto ice surfaces. Cryst Growth Des 3:747–752

    Article  CAS  Google Scholar 

  243. Deller RC, Vatish M, Mitchell DA, Gibson MI (2014) Synthetic polymers enable non-vitreous cellular cryopreservation by reducing ice crystal growth during thawing. Nat Commun 5:3244

    Article  PubMed  CAS  Google Scholar 

  244. Tan X, Song E, Liu X, Liu G, Cheng H, Wan F (2012) Successful vitrification of mouse ovaries using less-concentrated cryoprotectants with supercool X-1000 supplementation. In Vitro Cell Dev Biol Anim 48:69–74

    Article  PubMed  Google Scholar 

  245. Fahy GM, Wowk B, Wu J, Paynter S (2004) Improved vitrification solutions based on predictability of vitrification solution toxicity. Cryobiology 48:22–35

    Article  CAS  PubMed  Google Scholar 

  246. Ting AY, Yeoman RR, Lawson MS, Zelinski MB (2012) Synthetic polymers improve vitrification outcomes of macaque ovarian tissue as assessed by histological integrity and the in vitro development of secondary follicles. Cryobiology 65:1–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Pichugin Y, Fahy GM, Morin R (2006) Cryopreservation of rat hippocampal slices by vitrification. Cryobiology 52:228–240

    Article  CAS  PubMed  Google Scholar 

  248. Fahy GM, Guan N, De Graaf IAM, Tan Y, Griffin L, Groothuis GMM (2013) Cryopreservation of precision-cut tissue slices. Xenobiotica 43:113–132

    Article  CAS  PubMed  Google Scholar 

  249. Ting AY, Yeoman RR, Campos JR, Lawson MS, Mullen SF, Fahy GM, Zelinski MB (2013) Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system. Hum Reprod 28:1267–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Kami D, Kasuga J, Arakawa K, Fujikawa S (2008) Improved cryopreservation by diluted vitrification solution with supercooling-facilitating flavonol glycoside. Cryobiology 57:242–245

    Article  CAS  PubMed  Google Scholar 

  251. Biggs CI, Bailey TL, Graham B, Stubbs C, Fayter A, Gibson MI (2017) Polymer mimetics of biomacromolecular antifreezes. Nat Commun 8:1546

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  252. Matsumura K, Hyon SH (2009) Polyampholytes as low toxic efficient cryoprotective agents with antifreeze protein properties. Biomaterials 30:4842–4849

    Article  CAS  PubMed  Google Scholar 

  253. Matsumura K, Bae JY, Hyon SH (2010) Polyampholytes as cryoprotective agents for mammalian cell cryopreservation. Cell Transplant 19:691–699

    Article  PubMed  Google Scholar 

  254. Matsumura K, Bae JY, Kim HH, Hyon SH (2011) Effective vitrification of human induced pluripotent stem cells using carboxylated επσιλον-πολψ-Λ-λψσινε. Cryobiology 63:76–83

    Article  CAS  PubMed  Google Scholar 

  255. Maehara M, Sato M, Watanabe M, Matsunari H, Kokubo M, Kanai T, Sato M, Matsumura K, Hyon SH, Yokoyama M, Mochida J, Nagashima H (2013) Development of a novel vitrification method for chondrocyte sheets. BMC Biotechnol 13:58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  256. Shibao Y, Fujiwara K, Kawasaki Y, Matsumura K, Hyon SH, Kashiwazaki N (2014) The effect of a novel cryoprotective agent, carboxylated epsilon-poly-l-lysine, on the developmental ability of re-vitrified mouse embryos at the pronuclear stage. Cryobiology 68:200–204

    Article  CAS  PubMed  Google Scholar 

  257. Watanabe H, Kohaya N, Kamoshita M, Fujiwara K, Matsumura K, Hyon SH, Ito J, Kashiwazaki N (2013) Efficient production of live offspring from mouse oocytes vitrified with a novel cryoprotective agent, carboxylated epsilon-L-lysine. PLoS One 8:e83613

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  258. Jimenez-Rios JL, Rabin Y (2006) Thermal expansion of blood vessels in low cryogenic temperatures, part II: Vitrification with VS55, DP6, and 7.05M DMSO. Cryobiology 52:284–294

    Article  PubMed Central  CAS  Google Scholar 

  259. Rabin Y, Steif PS, Hess JL, Jimenez-Rios JL, Palastro MC (2006) Fracture formation in vitrified thin films of cryoprotectants. Cryobiology 53:75–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  260. Pegg DE, Wusteman MC, Boylan S (1997) Fractures in cryopreserved elastic arteries. Cryobiology 34:183–192

    Article  CAS  PubMed  Google Scholar 

  261. Steif PS, Palastro MC, Rabin Y (2007) The effect of temperature gradients on stress development during cryopreservation via vitrification. Cell Preserv Technol. 5:104–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  262. Nei T (1976) Freezing injury to erythrocytes. I. Freezing patterns and post-thaw hemolysis. Cryobiology 13:278–286

    Article  CAS  PubMed  Google Scholar 

  263. Levin R, Cravalho EG, Huggins CE (1977) Effect of solution non-ideality on erythrocyte volume regulation. Biochim Biophys Acta 465:179–190

    Article  CAS  PubMed  Google Scholar 

  264. Meryman HT (1966) Review of biological freezing. In: Meryman HT (ed) Cryobiology. Academic Press, New York, pp 1–114

    Google Scholar 

  265. Henniker JC, McBain JW (1948) The depth of the surface zone of a liquid. Vol. technical report no. 5, N60ri-154-T.O. II. Stanford Research Institute, Stanford

    Google Scholar 

  266. Vogler EA (1998) Structure and reactivity of water at biomaterial surfaces. Adv Colloid Interf Sci 74:69–117

    Article  CAS  Google Scholar 

  267. Isachenko E, Isachenko V, Katkov II, Sanchez R, van der Ven H, Nawroth F (2007) Cryoprotectant-free vitrification of spermatozoa. In: Tucker MJ, Liebermann J (eds) Vitrification in Assisted Reproduction, A User's Manual and Trouble-Shooting Guide. Informa Healthcare, London, pp 87–105

    Chapter  Google Scholar 

  268. Morris GJ, Acton E, Murray BJ, Fonseca F (2012) Freezing injury: the special case of the sperm cell. Cryobiology 64:71–80

    Article  CAS  Google Scholar 

  269. Nawroth F, Isachenko V, Dessole S, Rahimi G, Farina M, Vargiu N, Mallmann P, Dattena M, Capobianco G, Peters D, Orth I, Isachenko E (2002) Vitrification of human spermatozoa without cryoprotectants. Cryo-Letters 23:93–102

    CAS  PubMed  Google Scholar 

  270. Isachenko E, Isachenko V, Katkov II, Rahimi G, Schondorf T, Mallmann P, Dessole S, Nawroth F (2004) DNA integrity and motility of human spermatozoa after standard slow freezing versus cryoprotectant-free vitrification. Hum Reprod 19:932–939

    Article  CAS  PubMed  Google Scholar 

  271. Isachenko V, Isachenko E, Katkov II, Montag M, Dessole S, Nawroth F, Van der Ven H (2004) Cryoprotectant-free cryopreservation of human spermatozoa by vitrification and freezing in vapor: effect on motility, DNA integrity, and fertilization ability. Biol Reprod 71:1167–1173

    Article  CAS  PubMed  Google Scholar 

  272. Merino O, Sanchez R, Risopatron J, Isachenko E, Katkov II, Figueroa E, Valdebenito I, Mallmann P, Isachenko V (2012) Cryoprotectant-free vitrification of fish (Oncorhynchus mykiss) spermatozoa: first report. Andrologia 44(Suppl 1):390–395

    Article  PubMed  CAS  Google Scholar 

  273. Sherman JK, Kiu KC (1982) Ultrastructure before freezing, while frozen, and after thawing in assessing cryoinjury of mouse epididymal spermatozoa. Cryobiology 19:503–510

    Article  Google Scholar 

  274. Morris GJ (2006) Rapidly cooled human sperm: no evidence of intracellular ice formation. Hum Reprod 21:2075–2083

    Article  CAS  PubMed  Google Scholar 

  275. Isachenko V, Soler C, Isachenko E, Perez-Sanchez F, Grishchenko V (1998) Vitrification of immature porcine oocytes: effects of lipid droplets, temperature, cytoskeleton, and addition and removal of cryoprotectant. Cryobiology 36:250–253

    Article  CAS  PubMed  Google Scholar 

  276. He X, Park EYH, Fowler A, Yarmush ML, Toner M (2008) Vitrification by ultra-fast cooling at a low concentration of cryoprotectants in a quartz micro-capillary: a study using murine embryonic stem cells. Cryobiology 56:223–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  277. Asahina E, Shimada K, Hisada Y (1970) A stable state of frozen protoplasm with invisible intracellular ice crystals obtained by rapid cooling. Exp Cell Res 59:349–358

    Article  CAS  PubMed  Google Scholar 

  278. Takahashi T, Hirsh A, Erbe E, Williams RJ (1988) Mechanism of cryoprotection by extracellular polymeric solutes. Biophys J 54:509–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. MacFarlane DR (1987) Physical aspects of vitrification in aqueous solutions. Cryobiology 24:181–195

    Article  Google Scholar 

  280. Kleinhans FW, Mazur P (2015) Physical parameters, modeling, and methodological details in using IR laser pulses to warm frozen or vitrified cells ultra-rapidly. Cryobiology 70:195–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. Mazur P, Paredes E (2016) Roles of intracellular ice formation, vitrification of cell water, and recrystallisation of intracellular ice on the survival of mouse embryos and oocytes. Reprod Fertil Dev. https://doi.org/10.1071/RD16021

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

    Article  CAS  PubMed  Google Scholar 

  283. Clark P, Fahy GM, Karow AM Jr (1984) Factors influencing renal cryopreservation. II. Toxic effects of three cryoprotectants in combination with three vehicle solutions in non-frozen rabbit cortical slices. Cryobiology 21:274–284

    Article  CAS  PubMed  Google Scholar 

  284. Karow AM Jr, McDonald M, Dendle T, Rao R (1986) Functional preservation of the mammalian kidney. VII. Autologous transplantation of dog kidneys after treatment with dimethylsulfoxide (2.8 and 4.2 M). Transplantation 41:669–674

    Article  CAS  PubMed  Google Scholar 

  285. Pegg DE, Jacobsen IA, Diaper MP, Foreman J (1986) Optimization of a vehicle solution for the introduction and removal of glycerol with rabbit kidneys. Cryobiology 23:53–63

    Article  CAS  PubMed  Google Scholar 

  286. Meryman HT, Douglas MSJ (1982) Isotonicity in the presence of penetrating cryoprotectants. Cryobiology 19:565–569

    Article  CAS  Google Scholar 

  287. Meryman HT (2007) Cryopreservation of living cells: principles and practice. Transfusion 47:935–945

    Article  CAS  PubMed  Google Scholar 

  288. Nobel PS (1969) The Boyle-Van't Hoff relation. J Theor Biol 23:375–379

    Article  CAS  PubMed  Google Scholar 

  289. Vian AM, Higgins AZ (2014) Membrane permeability of the human granulocyte to water, dimethyl sulfoxide, glycerol, propylene glycol and ethylene glycol. Cryobiology 68:35–42

    Article  CAS  PubMed  Google Scholar 

  290. Mullen SF, Li M, Li Y, Chen ZJ, Critser JK (2008) Human oocyte vitrification: the permeability of metaphase II oocytes to water and ethylene glycol and the appliance toward vitrification. Fertil Steril 89:1812–1825

    Article  PubMed  Google Scholar 

  291. Jin B, Higashiyama R, Nakata Y, Yonezawa J, Xu S, Miyake M, Takahashi S, Kikuchi K, Yazawa K, Mizobuchi S, Kitayama M, Koshimoto C, Matsukawa K, Kasai M, Edashige K (2013) Rapid movement of water and cryoprotectants in pig expanded blastocysts via channel processes: its relevance to their higher tolerance to cryopreservation. Biol Reprod 89:87. [epub ahead of print]

    Article  PubMed  CAS  Google Scholar 

  292. Kleinhans FW (1998) Membrane permeability modeling: Kedem-Katchalsky vs a two-parameter formalism. Cryobiology 37:271–289

    Article  CAS  PubMed  Google Scholar 

  293. Levin R, Miller TW (1981) An optimum method for the introduction or removal of permeable cryoprotectants: isolated cells. Cryobiology 18:32–48

    Article  CAS  PubMed  Google Scholar 

  294. Levin R (1982) A generalized method for the minimization of cellular osmotic stresses and strains during the introduction and removal of permeable cryoprotectants. J Biomech Eng 104:81–86

    Article  CAS  PubMed  Google Scholar 

  295. Fahy GM, Lilley TH, Linsdell H, St. John Douglas M, Meryman HT (1990) Cryoprotectant toxicity and cryoprotectant toxicity reduction: in search of molecular mechanisms. Cryobiology 27:247–268

    Article  CAS  PubMed  Google Scholar 

  296. Fahy GM (2005) Vitrification as an approach to cryopreservation: general perspectives. Cryobiology 51:348–349

    Google Scholar 

  297. Wowk B, Darwin M, Harris SB, Russell SR, Rasch CM (1999) Effects of solute methoxylation on glass-forming ability and stability of vitrification solutions. Cryobiology 39:215–227

    Article  CAS  PubMed  Google Scholar 

  298. Benson JD, Kearsley AJ, Higgins AZ (2012) Mathematical optimization of procedures for cryoprotectant equilibration using a toxicity cost function. Cryobiology 64:144–151

    Article  CAS  PubMed  Google Scholar 

  299. Karlsson JO, Szurek EA, Higgins AZ, Lee SR, Eroglu A (2013) Optimization of cryoprotectant loading into murine and human oocytes. Cryobiology 68:18–28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  300. Benson JD, Higgins AZ, Desai K, Eroglu A (2018) A toxicity cost function approach to optimal CPA equilibration in tissues. Cryobiology 80:144–155

    Article  PubMed  Google Scholar 

  301. Ghousifam N, Sandoval B, Rylander MN (2019) Heat shock proteins as a potential tool to protect cells integrity during organ cryopreservation (abstract S44). Cryobiology. (in press)

    Google Scholar 

  302. Cypser JR, Chick WS, Fahy GM, Schumacher GJ, Johnson TE (2019) Genetic suppression of cryoprotectant toxicity. Cryobiology 86:95–102

    Article  CAS  PubMed  Google Scholar 

  303. Fahy GM (2019) Further optimization of organ perfusion with cryoprotective agents. Cryobiology. (in press)

    Google Scholar 

  304. Fahy GM (2016) Elimination of most damage after perfusing rabbit kidneys with M22 solutions. Cryobiology 73:407

    Article  Google Scholar 

  305. Franks F, Mathias SF, Galfre P, Webster SD, Brown D (1983) Ice nucleation and freezing in undercooled cells. Cryobiology 20:298–309

    Article  CAS  PubMed  Google Scholar 

  306. Fink AL (1986) Effects of cryoprotectants on enzyme structure. Cryobiology 23:28–37

    Article  CAS  PubMed  Google Scholar 

  307. Jans AWH, Willem R (1988) 13C-NMR study of glycerol metabolism in rabbit renal cells of proximal convoluted tubules. Eur J Biochem 174:67–73

    Article  CAS  PubMed  Google Scholar 

  308. Sestoft L, Fleron P (1975) Kinetics of glycerol uptake by the perfused rat liver: membrane transport, phosphorylation and effect on NAD redox level. Biochim Biophys Acta 375:462–471

    Article  CAS  PubMed  Google Scholar 

  309. Blow AM, Botham GM, Fisher D, Goodall AH, Tilcock CP, Lucy JA (1978) Water and calcium ions in cell fusion induced by poly(ethylene glycol). FEBS Lett 94:305–310

    Article  CAS  PubMed  Google Scholar 

  310. Shaw JM, Kuleshova LL, MacFarlane DR, Trounson AO (1997) Vitrification properties of solutions of ethylene glycol in saline containing PVP, ficoll, or dextran. Cryobiology 35:219–229

    Article  CAS  PubMed  Google Scholar 

  311. Kuleshova LL, MacFarlane DR, Trounson AO, Shaw JM (1999) Sugars exert a major influence on the vitrification properties of ethylene glycol-based solutions and have low toxicity to embryos and oocytes. Cryobiology 38:119–130

    Article  CAS  PubMed  Google Scholar 

  312. Fahy GM, da Mouta C, Tsonev L, Khirabadi BS, Mehl P, Meryman HT (1995) Cellular injury associated with organ cryopreservation: chemical toxicity and cooling injury. In: Lemasters JJ, Oliver C (eds) Cell Biology of Trauma. CRC Press, Boca Raton

    Google Scholar 

  313. Fahy GM (2010) Cryoprotectant toxicity neutralization. Cryobiology 60:S45–S53

    Article  CAS  PubMed  Google Scholar 

  314. Yancey PG, Clark ME, Hand SC, Rowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222

    Article  CAS  PubMed  Google Scholar 

  315. Somero GN (1986) From dogfish to dogs: Trimethylamines protect proteins from urea. News Physiol Sci 1:9–12

    CAS  Google Scholar 

  316. Wang A, Bolen DW (1997) A naturally occurring protective system in urea-rich cells: mechanisms of osmolyte protection of proteins against urea denaturation. Biochemistry 36:9101–9108

    Article  CAS  PubMed  Google Scholar 

  317. Lin TY, Timasheff SN (1994) Why do some organisms use a urea-methylamine mixture as osmolyte? Thermodynamic compensation of urea and trimethylamine N-oxide interactions with protein. Biochemistry 33:12695–12701

    Article  CAS  PubMed  Google Scholar 

  318. Baxter S, Lathe G (1971) Biochemical effects on kidney of exposure to high concentrations of dimethyl sulphoxide. Biochem Pharmacol 30:1079–1091

    Article  Google Scholar 

  319. Mirsalikhova NM (1978) Stabilizatsiia Na+,K+-adenozintrifosfatazy dimetilsulfoxsidom pri inaktivatsii mochevinoi. Biokhimiia 43:34–39

    CAS  PubMed  Google Scholar 

  320. Anchordoguy TJ, Carpenter JF, Crowe JH, Crowe LM (1992) Temperature-dependent perturbation of phospholipid bilayers by dimethylsulfoxide. Biochim Biophys Acta 1104:117–122

    Article  CAS  PubMed  Google Scholar 

  321. Rajesh, K., Oh, K., and Baiz, C.R. (2020) Amides modulate protein stability in dimethyl sulfoxide (DMSO) solutions. (in preparation)

    Google Scholar 

  322. Shlafer M, Matheny JL, Karow AM Jr (1976) Cardiac chronotropic mechanisms of dimethyl sulfoxide: inhibition of acetylcholinesterase and antagonism of negative chronotropy by atropine. Arch Int Pharmacodyn Ther 221:21–31

    CAS  PubMed  Google Scholar 

  323. de Graaf IA, Draaisma AL, Schoeman O, Fahy GM, Groothuis GM, Koster HJ (2007) Cryopreservation of rat precision-cut liver and kidney slices by rapid freezing and vitrification. Cryobiology 54:1–12

    Article  PubMed  CAS  Google Scholar 

  324. Burch HB, Lowry OH, Meinhardt L, Max P, Chyu K-J (1970) Effect of fructose, dihydroxyacetone, glycerol and sucrose on metabolites and related compounds in liver and kidney. J Biol Chem 245:2092–2102

    Article  CAS  PubMed  Google Scholar 

  325. Booth ED, Dofferhoff O, Boogaard PJ, Watson WP (2004) Comparison of the metabolism of ethylene glycol and glycolic acid in vitro by precision-cut tissue slices from female rat, rabbit, and human liver. Xenobiotica 34:31–48

    Article  CAS  PubMed  Google Scholar 

  326. Leth PM, Gregersen M (2005) Ethylene glycol poisoning. Forensic Sci Int 155:179–184

    Article  CAS  PubMed  Google Scholar 

  327. Jacob SW, Herschler R (1986) Pharmacology of DMSO. Cryobiology 23:14–27

    Article  CAS  PubMed  Google Scholar 

  328. Snow JT, Finley JW, Friedman M (1975) Oxidation of sulfhydryl groups to disulfides by sulfoxides. Biochem Biophys Res Commun 64:441–447

    Article  CAS  PubMed  Google Scholar 

  329. Agarwal SP, Nwaiwu J (1984) Dimethyl sulfoxide as a spray reagent for the detection of triterpenoids and some steroids on thin-layer plates. J Chromatogr 295:537–542

    Article  CAS  Google Scholar 

  330. Friend C, Scher W, Preisler HD, Holland JG (1973) Studies on erythroid differentiation of Friend virus-induced murine leukemia cells. Bibl Haematol 39:916–923

    CAS  PubMed  Google Scholar 

  331. Reboulleau CP, Shapiro HS (1983) Chemical inducers of differentiation cause conformational changes in the chromatin and deoxyribonucleic acid of murine erythroleukemia cells. Biochemistry 22:4512–4517

    Article  CAS  PubMed  Google Scholar 

  332. Arakawa T, Kita Y, Timasheff SN (2007) Protein precipitation and denaturation by dimethyl sulfoxide. Biophys Chem 131:62–70

    Article  CAS  PubMed  Google Scholar 

  333. Gekko K, Timasheff SN (1981) Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures. Biochemistry 20:4667–4676

    Article  CAS  PubMed  Google Scholar 

  334. Arakawa T, Timasheff SN (1982) Stabilization of protein structure by sugars. Biochemistry 21:6536–6544

    Article  CAS  PubMed  Google Scholar 

  335. Timasheff SN (2002) Protein hydration, thermodynamic binding, and preferential hydration. Biochemistry 41:13473–13482

    Article  CAS  PubMed  Google Scholar 

  336. Kim SH, Yan YB, Zhou HM (2006) Role of osmolytes as chemical chaperones during the refolding of aminoacylase. Biochem Cell Biol 84:30–38

    Article  CAS  PubMed  Google Scholar 

  337. Hamagushi K (1964) Structure of muramidase (lysozyme). VIII. Effect of dimethyl sulfoxide on the stability of muramidase. J Biochem 56:441–449

    Google Scholar 

  338. Fujita Y, Izumiguchi S, Noda Y (1982) Effect of dimethylsulfoxide and its homologues on the thermal denaturation of lysozyme as measured by differential scanning calorimetry. J Peptide Prot Res 19:25–31

    Article  CAS  Google Scholar 

  339. Arakawa T (1990) The basis for toxicity of certain cryoprotectants: a hypothesis. Cryobiology 27:401–415

    Article  CAS  Google Scholar 

  340. Strambini GB, Balestreri E, Galli A, Gonnelli M (2008) Effects of sugars and polyols on the stability of azurin in ice. J Phys Chem B 112:4372–4380

    Article  CAS  PubMed  Google Scholar 

  341. MacFarlane DR, Forsyth M (1990) Recent insights on the role of cryoprotective agents in vitrification. Cryobiology 27:345–358

    Article  CAS  Google Scholar 

  342. Yoshida T, Maulik N, Ho YS, Alam J, Das DK (2001) H(mox-1) constitutes an adaptive response to effect antioxidant cardioprotection: a study with transgenic mice heterozygous for targeted disruption of the Heme oxygenase-1 gene. Circulation 103:1695–1701

    Article  CAS  PubMed  Google Scholar 

  343. Hayakawa K, Hiramatsu N, Okamura M, Yao J, Paton AW, Paton JC, Kitamura M (2008) Blunted activation of NF-kappaB and NF-kappaB-dependent gene expression by geranylgeranylacetone: involvement of unfolded protein response. Biochem Biophys Res Commun 365:47–53

    Article  CAS  PubMed  Google Scholar 

  344. Wang Z, Gall JM, Bonegio RG, Havasi A, Hunt CR, Sherman MY, Schwartz JH, Borkan SC (2011) Induction of heat shock protein 70 inhibits ischemic renal injury. Kidney Int 79:861–870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  345. Arakawa T, Bhat R, Timasheff SN (1990) Why preferential hydration does not always stabilize the native structure of globular proteins. Biochemistry 29:1924–1931

    Article  CAS  PubMed  Google Scholar 

  346. Farrant J (1965) Permeability of Guinea-pig smooth muscle to non-electrolytes. J Physiol 178:1–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  347. Fahy GM (1980) Analysis of "solution effects" injury: rabbit renal cortex frozen in the presence of dimethyl sulfoxide. Cryobiology 17:371–388

    Article  CAS  PubMed  Google Scholar 

  348. Tedesco PM, Schumacher GJ, Johnson TJ (2019) Cryoprotectant toxicity in Caenorhabditis elegans. Cryobiology 86:71–76

    Article  CAS  PubMed  Google Scholar 

  349. Sonna LA, Fujita J, Gaffin SI, Lilly CM (2002) Effects of heat and cold stress on mammalian gene expression. J Appl Physiol 92:1725–1742

    Article  CAS  PubMed  Google Scholar 

  350. Al-Fageeh MB, Marchant RJ, Carden MJ, Smales CM (2006) The cold shock response in cultured mammalian cells: harnessing the response for the improvement of recombinant protein production. Biotechnol Bioeng 93:829–835

    Article  CAS  PubMed  Google Scholar 

  351. Inouye M, Yamanaka K (2000) Cold Shock Response and Adaptation. Horizon Scientific Press, Norfolk

    Google Scholar 

  352. Lyons JM, Raison JK (1970) Oxidation activity of mitochondria isolated from plant tissue sensitive and resistant to chilling injury. Plant Physiol 45:386–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  353. Lyons JM (1972) Phase transitions and control of cellular metabolism at low temperatures. Cryobiology 9:341–350

    Article  CAS  PubMed  Google Scholar 

  354. Ghetler Y, Yavin S, Shalgi R, Arav A (2005) The effect of chilling on membrane lipid phase transition in human oocytes and zygotes. Hum Reprod 20:3385–3389

    Article  CAS  PubMed  Google Scholar 

  355. Drobnis EZ, Crowe LM, Berger T, Anchordoguy TJ, Overstreet JW, Crowe JH (1993) Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. J Exp Zool 265:432–437

    Article  CAS  PubMed  Google Scholar 

  356. Hays LM, Feeney RE, Crowe LM, Crowe JH, Oliver AE (1996) Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic phase transitions. Proc Natl Acad Sci U S A 93:6835–6840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  357. Hays LM, Crowe JH, Wolkers W, Rudenko S (2001) Factors affecting leakage of trapped solutes from phospholipid vesicles during thermotropic phase transitions. Cryobiology 42:88–102

    Article  CAS  PubMed  Google Scholar 

  358. He L, Bailey JL, Buhr MM (2001) Incorporating lipids into boar sperm decreases chilling sensitivity but not capacitation potential. Biol Reprod 64:69–79

    Article  CAS  PubMed  Google Scholar 

  359. Horvath G, Seidel GE Jr (2006) Vitrification of bovine oocytes after treatment with cholesterol-loaded methyl-beta-cyclodextrin. Theriogenology 66:1026–1033

    Article  CAS  PubMed  Google Scholar 

  360. Tomczak MM, Hincha DK, Estrada SD, Wolkers WF, Crowe LM, Feeney RE, Tablin F, Crowe JH (2002) A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophys J 82:874–881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  361. Wada H, Gombos Z, Murata N (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature 347:200–203

    Article  CAS  PubMed  Google Scholar 

  362. Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713

    Article  CAS  Google Scholar 

  363. Burton V, Mitchell HK, Young P, Petersen NS (1988) Heat shock protection against cold stress of Drosophila melanogaster. Mol Cell Biol 8:3550–3552

    CAS  PubMed  PubMed Central  Google Scholar 

  364. VanBogelen RA, Neidhardt FC (1990) Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A 87:5589–5593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  365. Schindelin H, Marahiel MA, Heinemann U (1993) Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364:164–168

    Article  CAS  PubMed  Google Scholar 

  366. Corwin WL, Baust JM, Baust JG, Van Buskirk RG (2011) The unfolded protein response in human corneal endothelial cells following hypothermic storage: implications of a novel stress pathway. Cryobiology 63:46–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  367. Takahashi T, Hammett MF, Cho MS (1985) Multifaceted freezing injury in human polymorphonuclear cells at high subfreezing temperatures. Cryobiology 22:215–236

    Article  CAS  PubMed  Google Scholar 

  368. Zhou GB, Li N (2009) Cryopreservation of porcine oocytes: recent advances. Mol Hum Reprod 15:279–285

    Article  CAS  PubMed  Google Scholar 

  369. Zhang W, Yi K, Yan H, Zhou X (2012) Advances on in vitro production and cryopreservation of porcine embryos. Anim Reprod Sci 132:115–122

    Article  CAS  PubMed  Google Scholar 

  370. Cameron RD, Beebe LF, Blackshaw AW (2006) Cryopreservation and transfer of pig embryos. Soc Reprod Fertil Suppl 62:277–291

    CAS  PubMed  Google Scholar 

  371. Nagashima H, Hiruma K, Saito H, Tomii R, Ueno S, Nakayama N, Matsunari H, Kurome M (2007) Production of live piglets following cryopreservation of embryos derived from in vitro-matured oocytes. Biol Reprod 76:900–905

    Article  CAS  PubMed  Google Scholar 

  372. Beeb LF, Cameron RD, Blackshaw AW, Higgins A, Nottle MB (2002) Piglets born from centrifuged and vitrified early and peri-hatching blastocysts. Theriogenology 57:2155–2165

    Article  CAS  PubMed  Google Scholar 

  373. Pickering SJ, Johnson MH (1987) The influence of cooling on the organization of the meiotic spindle of the mouse oocyte. Hum Reprod 2:207–216

    Article  CAS  PubMed  Google Scholar 

  374. Wang WH, Meng L, Hackett RJ, Odenbourg R, Keefe DL (2001) Limited recovery of meiotic spindles in living human oocytes after cooling-rewarming observed using polarized light microscopy. Hum Reprod 16:2374–2378

    Article  CAS  PubMed  Google Scholar 

  375. Yang D, Winslow KL, Nguyen K, Duffy D, Freeman M, Al-Shawaf T (2010) Comparison of selected cryoprotective agents to stabilize meiotic spindles of human oocytes during cooling. J Exp Clin Assist Reprod 7:4

    PubMed Central  Google Scholar 

  376. Mandelbaum J, Anastasiou O, Levy R, Guerin J-F, de Larouziere V, Antoine JM (2004) Effects of cryopreservation on the meiotic spindle of human oocytes. Eur J Obstet Gynecol Reprod Biol 113(Suppl 1):S17–S23

    Article  PubMed  Google Scholar 

  377. McGrath JJ (1989) Protecting biological material against chilling injury, in European Patent Office

    Google Scholar 

  378. Fahy GM (2007) Hypertonic reduction of chilling injury, USPTO, 21st century medicine, Inc.: United States

    Google Scholar 

  379. Rowe AW (1987) Sixteen year cryogenic storage of blood frozen by droplet freezing technique and a low glycerol-rapid freeze procedure. In: Proc XVII Intern Congress Refrigeration. Internatl Inst Refrigeration, Paris, pp 135–140

    Google Scholar 

  380. Valeri CR, Pivacek LE (1996) Effects of the temperature, the duration of frozen storage, and the freezing container on in vitro measurements in human peripheral blood mononuclear cells. Transfusion 36:303–308

    Article  CAS  PubMed  Google Scholar 

  381. Valeri CR, Pivacek LE, Gray AD, Cassidy GP, Leavy ME, Dennis RC, Melaragno AJ, Niehoff J, Yeston N, Emerson CP, Altschule MD (1989) The safety and therapeutic effectiveness of human red cells stored at -80°C for as long as 21 years. Transfusion 29:429–437

    Article  CAS  PubMed  Google Scholar 

  382. Song YC, Li CY, Lightfoot FG, Boggs JM, Greene ED, Taylor MJ, Chen ZZ, Brockbank KGM (2002) Stability of vitrified tissues in the vapor phase of liquid nitrogen. Cryobiology 45:243

    Google Scholar 

  383. Sun WQ, Leopold AC, Crowe LM, Crowe JH (1996) Stability of dry liposomes in sugar glasses. Biophys J 70:1769–1776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  384. Walters C (2004) Temperature dependency of molecular mobility in preserved seeds. Biophys J 86:1253–1258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  385. Walters C (2004) Longevity of cryogenically stored seeds. Cryobiology 48:229–244

    Article  PubMed  Google Scholar 

  386. Shamblin SL, Tang X, Chang LJ, Hancock BC, Pikal MJ (1999) Characterization of the time scales of molecular motion in pharmacologically important glasses. J Phys Chem B 103:4113–4121

    Article  CAS  Google Scholar 

  387. Ashwood-Smith MJ, Grant E (1977) Genetic stability in cellular systems in the frozen state. In: Elliott K, Whelan J (eds) The freezing of mammalian embryos. Elsevier/Excepta Medica, North-Holland Amsterdam, pp 251–267

    Google Scholar 

  388. Lyon MF, Glenister PH, Whittingham DG (1981) Long-term viability of embryos stored under irradiation. In: Zeilmaker GH (ed) Frozen storage of laboratory animals. Gustav Fischer Verlag, Stuttgart, pp 139–147

    Google Scholar 

  389. Fink AL (1979) Enzyme-catalyzed reactions in unfrozen, noncellular systems at subzero temperatures. In: Fennema O (ed) Proteins at low temperatures. American Chemical Society, Washington, DC, pp 35–54

    Chapter  Google Scholar 

  390. Douzou P (1977) Cryobiochemistry, an introduction. Academic Press, New York

    Google Scholar 

  391. Brandts JF, Fu J, Nordin JH (1970) The low temperature denaturation of chymotrypsinogen in aqueous solution and in frozen aqueous solution. In: Wolstenholme GEW, O'Connor M (eds) The frozen cell. J & A Churchill, London, pp 189–209

    Google Scholar 

  392. Dias CL, Ala-Nissila T, Wong-ekkabut J, Vattulainen I, Grant M, Karttunen M (2010) The hydrophobic effect and its role in cold denaturation. Cryobiology 60:91–99

    Article  CAS  PubMed  Google Scholar 

  393. Lopez CF, Darst RK, Rossky PJ (2008) Mechanistic elements of protein cold denaturation. J Phys Chem B 112:5961–5967

    Article  CAS  PubMed  Google Scholar 

  394. Fennema O (1979) Proteins at low temperatures. In: Comstock MJ (ed) Advances in chemistry, vol 180. American Chemical Society, Washington

    Google Scholar 

Download references

Acknowledgments

Supported by 21st Century Medicine, Inc. We thank Mehmet Toner for bringing the work of Goetz and Goetz and of Stiles to our attention.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gregory M. Fahy .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Fahy, G.M., Wowk, B. (2021). Principles of Ice-Free Cryopreservation by Vitrification. In: Wolkers, W.F., Oldenhof, H. (eds) Cryopreservation and Freeze-Drying Protocols. Methods in Molecular Biology, vol 2180. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-0783-1_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-0783-1_2

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-0782-4

  • Online ISBN: 978-1-0716-0783-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics