Direct Measurement of Water States in Cryopreserved Cells Reveals Tolerance toward Ice Crystallization

Biophysical Journal

Volumn 110, Issue 4, 2016, Pages 840-849

  Huebinger, Jan ^a   Han, Hong Mei ^a   Hofnagel, Oliver ^a   Vetter, Ingrid R ^a   Bastiaens, Philippe I H ^a   Grabenbauer, Markus ^a,b  

^a MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ICE;

CELL SURVIVAL; CRYOELECTRON MICROSCOPY; CRYOPRESERVATION; CRYSTALLIZATION; HELA CELL LINE; HUMAN; PROCEDURES; X RAY DIFFRACTION;

CELL SURVIVAL; CRYOELECTRON MICROSCOPY; CRYOPRESERVATION; CRYSTALLIZATION; HELA CELLS; HUMANS; ICE; X-RAY DIFFRACTION;

EID: 84959491334     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.09.029     Document Type: Article

References (52)

1. D.E. Pegg Principles of cryopreservation Methods Mol. Biol. 368 2007 39 57
2. C.G. Salzmann, and P.G. Radaelli J.L. Finney The polymorphism of ice: five unresolved questions Phys. Chem. Chem. Phys. 13 2011 18468 18480
3. G. Malenkov Liquid water and ices: understanding the structure and physical properties J. Phys. Condens. Matter 21 2009 283101
4. T. Loerting, and K. Winkel D.T. Bowron How many amorphous ices are there? Phys. Chem. Chem. Phys. 13 2011 8783 8794
5. J. Dubochet Cryo-EM - the first thirty years J. Microsc. 245 2012 221 224
6. P. Mazur Kinetics of water loss from cells at subzero temperatures and the likelihood of intracellular freezing J. Gen. Physiol. 47 1963 347 369
7. D.E. Pegg The relevance of ice crystal formation for the cryopreservation of tissues and organs Cryobiology 60 3, Suppl 2010 S36 S44
8. J.E. Lovelock The mechanism of the protective action of glycerol against haemolysis by freezing and thawing Biochim. Biophys. Acta 11 1953 28 36
9. D.H. Edgar, and D.A. Gook A critical appraisal of cryopreservation (slow cooling versus vitrification) of human oocytes and embryos Hum. Reprod. Update 18 2012 536 554
10. W.F. Rall, and G.M. Fahy Ice-free cryopreservation of mouse embryos at -196 degrees C by vitrification Nature 313 1985 573 575
11. B. Wowk Thermodynamic aspects of vitrification Cryobiology 60 2010 11 22
12. G.M. Fahy, and B. Wowk Principles of cryopreservation by vitrification Methods Mol. Biol. 1257 2015 21 82
13. D.E. Pegg Principles of cryopreservation Methods Mol. Biol. 1257 2015 3 19
14. P. Mazur Freezing of living cells: mechanisms and implications Am. J. Physiol. 247 1984 C125 C142
15. J. Dubochet, and M. Adrian P. Schultz Cryo-electron microscopy of vitrified specimens Q. Rev. Biophys. 21 1988 129 228
16. J.B. Hopkins, and R. Badeau R.E. Thorne Effect of common cryoprotectants on critical warming rates and ice formation in aqueous solutions Cryobiology 65 2012 169 178
17. S. Seki, and P. Mazur Ultra-rapid warming yields high survival of mouse oocytes cooled to -196°c in dilutions of a standard vitrification solution PLoS One 7 2012 e36058
18. 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 59 2009 75 82
19. L.L. Kuleshova, and D.R. MacFarlane J.M. Shaw Sugars exert a major influence on the vitrification properties of ethylene glycol-based solutions and have low toxicity to embryos and oocytes Cryobiology 38 1999 119 130
20. C. Bouchet-Marquis, V. Starkuviene, and M. Grabenbauer Golgi apparatus studied in vitreous sections J. Microsc. 230 2008 308 316
21. P.B. Pedro, and S.E. Zhu M. Kasai Effects of hypotonic stress on the survival of mouse oocytes and embryos at various stages Cryobiology 35 1997 150 158
22. R. Gualtieri, and V. Mollo R. Talevi Ultrastructure and intracellular calcium response during activation in vitrified and slow-frozen human oocytes Hum. Reprod. 26 2011 2452 2460
23. J.R. Prentice-Biensch, and J. Singh M. Anzar Vitrification of immature bovine cumulus-oocyte complexes: effects of cryoprotectants, the vitrification procedure and warming time on cleavage and embryo development Reprod. Biol. Endocrinol. 10 2012 73
24. S. Hochi, and T. Terao M. Hirao Successful vitrification of pronuclear-stage rabbit zygotes by minimum volume cooling procedure Theriogenology 61 2004 267 275
25. G. Coticchio, and J.J. Bromfield D.F. Albertini Vitrification may increase the rate of chromosome misalignment in the metaphase II spindle of human mature oocytes Reprod. Biomed. Online 19 Suppl 3 2009 29 34
26. A.F.J. Beier, and J.C. Schulz H. Zimmermann Effective surface-based cryopreservation of human embryonic stem cells by vitrification Cryobiology 63 2011 175 185
27. H. Iwayama, and S. Hochi Y. Fukui Effects of cryodevice type and donors' sexual maturity on vitrification of minke whale (Balaenoptera bonaerensis) oocytes at germinal vesicle stage Zygote 12 2004 333 338
28. A. Al-Amoudi, L.P.O. Norlen, and J. Dubochet Cryo-electron microscopy of vitreous sections of native biological cells and tissues J. Struct. Biol. 148 2004 131 135
29. V. Tirtaatmadja, D.E. Dunstan, and D.V. Boger Rheology of dextran solutions J. Nonnewton. Fluid Mech. 97 2001 295 301
30. S. Cha, S.H. Kim, and D. Kim Viscosity of sucrose aqueous solutions measured by fluorescence correlation spectroscopy J. Korean Phys. Soc. 56 2010 1315 1318
31. T. Zamir, and A. Khan Study of ion-solvent interactions of lithium bromide in DMSO, H2O and DMSO-H2O mixtures at 25°C J. Chem. Soc. Pak. 27 2005 130 136
32. W. Hayduk, and V.K. Malik Density, viscosity, and carbon dioxide solubility and diffusivity in aqueous ethylene glycol solutions J. Chem. Eng. Data 16 1971 143 146
33. T.T. Herskovits, and T.M. Kelly Viscosity studies of aqueous solutions of alcohols, ureas, and amides J. Phys. Chem. 77 1973 381 388
34. J.L. Leunissen, and H. Yi Self-pressurized rapid freezing (SPRF): a novel cryofixation method for specimen preparation in electron microscopy J. Microsc. 235 2009 25 35
35. H.M. Han, J. Huebinger, and M. Grabenbauer Self-pressurized rapid freezing (SPRF) as a simple fixation method for cryo-electron microscopy of vitreous sections J. Struct. Biol. 178 2012 84 87
36. M. Grabenbauer, H.-M. Han, and J. Huebinger Cryo-fixation by self-pressurized rapid freezing Methods Mol. Biol. 1117 2014 173 191
37. J. Sun, and H. Li How to operate a cryo-electron microscope Methods Enzymol. 481 2010 231 249
38. J.R. Kremer, D.N. Mastronarde, and J.R. McIntosh Computer visualization of three-dimensional image data using IMOD J. Struct. Biol. 116 1996 71 76
39. D.N. Mastronarde Dual-axis tomography: an approach with alignment methods that preserve resolution J. Struct. Biol. 120 1997 343 352
40. E.F. Pettersen, and T.D. Goddard T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
41. G. Vajta, and P. Holm H. Callesen Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos Mol. Reprod. Dev. 51 1998 53 58
42. A. Arav Cryopreservation of oocytes and embryos Theriogenology 81 2014 96 102
43. E. Paredes, and P. Mazur The survival of mouse oocytes shows little or no correlation with the vitrification or freezing of the external medium, but the ability of the medium to vitrify is affected by its solute concentration and by the cooling rate Cryobiology 67 2013 386 390
44. D. Turnbull Under what conditions can a glass be formed? Contemp. Phys. 10 1969 473 488
45. S. Yavin, and A. Arav Measurement of essential physical properties of vitrification solutions Theriogenology 67 2007 81 89
46. J. Dubochet The physics of rapid cooling and its implications for cryoimmobilization of cells Methods Cell Biol. 79 2007 7 21
47. R. Spindler, W.F. Wolkers, and B. Glasmacher Dimethyl sulfoxide and ethylene glycol promote membrane phase change during cryopreservation Cryo Lett. 32 2011 148 157
48. M. Akhoondi, and H. Oldenhof W.F. Wolkers Membrane hydraulic permeability changes during cooling of mammalian cells Biochim. Biophys. Acta 1808 2011 642 648
49. K.R. Walters Jr., and A.S. Serianni J.G. Duman A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides Proc. Natl. Acad. Sci. USA 106 2009 20210 20215
50. M.I. Gibson Slowing the growth of ice with synthetic macromolecules: beyond antifreeze(glyco) proteins Polym. Chem. 1 2010 1141
51. A.K. Balcerzak, and S.S. Ferreira R.N. Ben Structurally diverse disaccharide analogs of antifreeze glycoproteins and their ability to inhibit ice recrystallization Bioorg. Med. Chem. Lett. 22 2012 1719 1721
52. S. Venketesh, and C. Dayananda Properties, potentials, and prospects of antifreeze proteins Crit. Rev. Biotechnol. 28 2008 57 82