The Thermodynamics of Water Transport From Biological Cells During Freezing

Silvares, O. M.; Cravalho, E.G.; Toscano, W. M.; Huggins, Charles

doi:10.1115/1.3450434

Cited by 37 publications

(16 citation statements)

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“…Although, the Lp measured at -5°C was similar for both nonacclimated and acclimated protoplasts, we suspect that impeded water efflux is occurring at the lower temperatures imposed on the acclimated protoplasts. This is suggested by theoretical considerations that reduced water efflux at low temperatures may occur due to the influence of temperature and increased osmolality on the hydraulic conductivity of the plasma membrane (8,22).…”

Section: Discussionmentioning

confidence: 99%

Effect of Cold Acclimation on Intracellular Ice Formation in Isolated Protoplasts

Dowgert¹,

Steponkus²

1983

Plant Physiol.

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When cooled at rapid rates to temperatures between -10 and -30°C, the incidence of intracellular ice formation was less in protoplasts enzymically isolated from cold acclimated leaves of rye (Secale cereale L. cv Puma) than that observed in protoplasts isolated from nonacclimated leaves. The extent of supercooling of the intracellular solution at any given temperature increased in both nonacclimated and acclimated protoplasts as the rate of cooling increased. There was no unique relationship between the extent of supercooling and the incidence of intracellular ice formation in either nonacclimated or acclimated protoplasts. In both nonacclimated and acclimated protoplasts, the extent of intracellular supercooling was snimlar under conditions that resulted in the greatest difference in the incidence of intracellular ice formation-cooling to -15 or -20°C at rates of 10 or 16'C/mitute. Further, the hydraulic conductivity determined during freeze-induced dehydration at -5°C was similar for both nonacclimated and acclimated protoplasts. A major distinction between nonacclimated and acclimated protoplasts was the temperature at which nucleation occurred. In nonacclimated protoplasts, nucleation occurred over a relatively narrow temperature range with a median nucleation temperature of -15°C, whereas in acclimated protoplasts, nucleation occurred over a broader temperature range with a median nucleation temperature of -42°C. We conclude that the decreased incidence of intracellular ice formation in acclimated protoplasts is attributable to an increase in the stability of the plasma membrane which precludes nucleation of the supercooled intracellular solution and is not attributable to an increase in hydraulic conductivity of the plasma membrane which purportedly precludes supercooling of the intracellular solution.It is commonly observed that the incidence of intracellular ice formation is a function of the cooling rate. As early as 1886, observed that rapid cooling resulted in intracellular ice formation whereas during slow cooling ice crystals were confined to extracellular spaces. Similar rates; and the higher the permeability to water, the lower the probability of intracellular ice formation. Further, because the deplasmolysis time of cells in cold hardy tissues was less than that for cells in nonhardy tissues, they inferred that water permeability increased following cold acclimation and that the incidence of intracellular ice formation would be less in acclimated tissues. In 1938, Siminovitch and Scarth (23) experimentally demonstrated that intracellular ice formation occurs less frequently in hardy tissues than nonhardy tissues when cooled at comparable rates. They too attributed this difference to the purported increase in water permeability of the plasma membrane following cold acclimation as proposed by Levitt and Scarth (10). Although this concept has been widely accepted and frequently cited, direct experimental verification of an increase in water permeability following cold acclimation has been...

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Section: Discussionmentioning

confidence: 99%

Effect of Cold Acclimation on Intracellular Ice Formation in Isolated Protoplasts

Dowgert¹,

Steponkus²

1983

Plant Physiol.

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“…The first of such models was due to Mazur in 1963. Mazur developed a mathematical model to predict the water content of cells subjected to freezing, the essence of which became the basis of almost all subsequent treatments (Mansoori, 1975;Silvares et al, 1975;Scheiwe & Koerber, 1983). Briefly, for a cell suspended in a freezing medium and subjected to sub-freezing temperatures, ice preferentially forms outside the cell in the freezing medium.…”

Section: Introductionmentioning

confidence: 99%

Water transport and estimated transmembrane potential during freezing of mouse oocytes

Toner

Cravalho

Armant³

1990

J. Membrain Biol.

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The kinetics of water transport and the changes in transmembrane potential during freezing of mouse oocytes in isotonic phosphate buffered saline (PBS) were simulated using thermodynamic models. The permeability to water at 0 degree C, Lpg, and the activation energy, ELp, of metaphase II mouse oocytes from B6D2F1 mice were determined to be 0.044 +/- 0.008 micron/min-atm and 13.3 +/- 2.5 kcal/mol during freezing at 2 degrees C/min. The inactive cell volume was determined to be 0.214 with a correlation coefficient of 0.995, indicating that the oocytes closely follow the ideal Boyle-van't Hoff relation. The mean value of the oocyte diameter was 79.41 +/- 4.62 microns. These results were used to predict the behavior of mouse oocytes under various freezing conditions. The effect of the cooling rate on the cell volume and cytoplasm undercooling was investigated. The changes in transmembrane potential were also investigated during freezing of mouse oocytes. The computer simulations showed that at the beginning of the freezing process (-1 degrees C), the fast growth of ice in the extracellular solution causes a sharp increase of the membrane potential. It is predicted that the change in membrane potential is substantial for almost all cooling rates. Estimations show that values as high as -90 mV may be reached during freezing. The hyperpolarization of the membrane may cause orientation of the dipoles within the membrane. For membrane proteins with 300 debye dipole moment, the theoretical prediction suggests that the percentage of dipoles aligned with the membrane potential increases from 16% at 0 degrees C prior to freezing to 58% at -8 degrees C after seeding of the external ice followed with a cooling at 120 degrees C/min.

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“…[71,72,112] and others), defined cryobiology as a science where much could be gained even by relatively simple models making broadly unrealistic assumptions. In fact as cryobiology has progressed as a discipline, various researchers have made use of models to determine optimal cooling and/or warming profiles [16,51,81,102,103,117,122], optimal pre-and post-cooling processing protocols [11,12,37,39,69,93,108], intracellular ice formation kinetics [3,45,46,119,125], ice damage in and optimal cryopreservation of tissues [1,2,23,31,99,111,114,126,127], among others.…”

Section: Introductionmentioning

confidence: 96%

Foundations of modeling in cryobiology—I: Concentration, Gibbs energy, and chemical potential relationships

Anderson¹,

Benson²,

Kearsley³

2014

Cryobiology

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The Thermodynamics of Water Transport From Biological Cells During Freezing

Cited by 37 publications

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Effect of Cold Acclimation on Intracellular Ice Formation in Isolated Protoplasts

Effect of Cold Acclimation on Intracellular Ice Formation in Isolated Protoplasts

Water transport and estimated transmembrane potential during freezing of mouse oocytes

Foundations of modeling in cryobiology—I: Concentration, Gibbs energy, and chemical potential relationships

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