DOI: 10.1002/jez.1402650413. Cold shock damage is due to lipid phase transitions in cell membranes: A demonstration using sperm as a model

Cold shock damage is due to lipid phase transitions in cell membranes: A demonstration using sperm as a model

10.1002/jez.1402650413

Crossref journal-article

Wiley

Journal of Experimental Zoology (311)

Abstract

AbstractWhen cells are cooled to temperatures above the freezing point of water at rates greater than a few degrees per minute, they sustain irreversible injury. Reduction of this “cold shock” damage could increase the survival of animals and plants at low environmental temperatures and improve the cryopreservation of plant and animal cells. Leakage of solutes across membranes, associated with thermotropic phase transitions in membrane lipids, is thought to be responsible, but this hypothesis has not been tested directly. Using Fourier transform infrared spectroscopy (FTIR), we measured the lipid phase transitions in intact, living sperm, the animal cell in which cold shock has been studied most extensively. A shift in the CH2 absorbance peaks indicates the transition from liquid‐crystalline to gel phase. The phase transition in sperm membranes occurred at a lower temperature for a marine shrimp than for the pig. In each case, potassium leakage, which is a hallmark of cold shock damage, increased abruptly near the end of the phase transition. Human sperm are quite resistant to cold shock, and an abrupt lipid phase transition was not detected. This phase behavior is typical of membranes containing a high proportion of cholesterol, and human sperm have an unusually high sterol content. High cholesterol levels are known to stabilize membranes during cooling. Overall, the lipid phase behavior was consistent with the temperature range over which cooling was damaging for pig and shrimp sperm, and the with the extent of damage produced in pig and human sperm. This is the first direct evidence that cold shock results from lipid phase transitions in cell membranes. © 1993 Wiley‐Liss, Inc.

Bibliography

Drobnis, E. Z., Crowe, L. M., Berger, T., Anchordoguy, T. J., Overstreet, J. W., & Crowe, J. H. (1993). Cold shock damage is due to lipid phase transitions in cell membranes: A demonstration using sperm as a model. Journal of Experimental Zoology, 265(4), 432â437. Portico.

Authors 6

Erma Z. Drobnis (first)
Lois M. Crowe (additional)
Trish Berger (additional)
Thomas J. Anchordoguy (additional)
James W. Overstreet (additional)
John H. Crowe (additional)

References 22 Referenced 423

10.1002/mrd.1120220405
10.1016/0005-2736(77)90026-8
{'key': 'e_1_2_1_4_1', 'first-page': '53', 'volume-title': 'Spectroscopy in the Biomedical Sciences', 'author': 'Cameron D. G.', 'year': '1986'} / Spectroscopy in the Biomedical Sciences by Cameron D. G. (1986)
10.1530/jrf.0.0850533
10.1016/0011-2240(89)90035-7
{'key': 'e_1_2_1_7_1', 'first-page': '39', 'volume-title': 'Membrane Fluidity in Biology', 'author': 'Cullis P. R.', 'year': '1983'} / Membrane Fluidity in Biology by Cullis P. R. (1983)
10.1016/0011-2240(90)90009-S
10.1002/j.1939-4640.1991.tb00250.x
10.1002/jez.1402300316
10.1530/jrf.0.0780447
{'key': 'e_1_2_1_12_1', 'first-page': '1', 'volume-title': 'Membrane Fluidity in Biology', 'author': 'Jain M. K.', 'year': '1983'} / Membrane Fluidity in Biology by Jain M. K. (1983)
{'key': 'e_1_2_1_13_1', 'first-page': '35', 'article-title': 'The effects of temperature on biological membranes and their models', 'volume': '41', 'author': 'Lee D. C.', 'year': '1987', 'journal-title': 'Symp. Soc. Exp. Biol.'} / Symp. Soc. Exp. Biol. / The effects of temperature on biological membranes and their models by Lee D. C. (1987)
{'key': 'e_1_2_1_14_1', 'first-page': '23', 'volume-title': 'Responses of Plants to Environmental Stresses', 'author': 'Levitt J.', 'year': '1980'} / Responses of Plants to Environmental Stresses by Levitt J. (1980)
{'key': 'e_1_2_1_15_1', 'first-page': '120', 'volume-title': 'The Effects of Low Temperatures on Biological Systems', 'author': 'Morris G. J.', 'year': '1987'} / The Effects of Low Temperatures on Biological Systems by Morris G. J. (1987)
{'key': 'e_1_2_1_16_1', 'first-page': '72', 'volume-title': 'The Effects of Low Temperatures on Biological Systems', 'author': 'Morris G. J.', 'year': '1987'} / The Effects of Low Temperatures on Biological Systems by Morris G. J. (1987)
{'key': 'e_1_2_1_17_1', 'first-page': '352', 'article-title': 'Cold shock injury—a comprehensive bibliography', 'volume': '5', 'author': 'Morris G. J.', 'year': '1984', 'journal-title': 'Cryo‐Lett.'} / Cryo‐Lett. / Cold shock injury—a comprehensive bibliography by Morris G. J. (1984)
10.1016/0005-2736(73)90314-3
10.1016/B978-0-12-053004-5.50008-X
{'key': 'e_1_2_1_20_1', 'first-page': '21', 'volume-title': 'Effects of Low Temperatures on Biological Membranes', 'author': 'Pringle M.', 'year': '1981'} / Effects of Low Temperatures on Biological Membranes by Pringle M. (1981)
10.1016/0011-2240(85)90167-1
{'key': 'e_1_2_1_22_1', 'first-page': '189', 'volume-title': 'Effects of Low Temperatures on Biological Membranes', 'author': 'Watson P. F.', 'year': '1981'} / Effects of Low Temperatures on Biological Membranes by Watson P. F. (1981)
{'key': 'e_1_2_1_23_1', 'first-page': '311', 'article-title': 'Cold shock injury in animal cells', 'volume': '41', 'author': 'Watson P. F.', 'year': '1987', 'journal-title': 'Proc. Soc. Exp. Biol.'} / Proc. Soc. Exp. Biol. / Cold shock injury in animal cells by Watson P. F. (1987)

Dates

Type	When
Created	20 years, 2 months ago (June 11, 2005, 5:12 a.m.)
Deposited	1 year, 10 months ago (Oct. 25, 2023, 3:26 a.m.)
Indexed	3 weeks, 1 day ago (Aug. 7, 2025, 4:54 a.m.)
Issued	32 years, 5 months ago (March 15, 1993)
Published	32 years, 5 months ago (March 15, 1993)
Published Online	20 years, 3 months ago (May 9, 2005)
Published Print	32 years, 5 months ago (March 15, 1993)

Funders 0

None

BibTeX

@article{Drobnis_1993, title={Cold shock damage is due to lipid phase transitions in cell membranes: A demonstration using sperm as a model}, volume={265}, ISSN={1097-010X}, url={http://dx.doi.org/10.1002/jez.1402650413}, DOI={10.1002/jez.1402650413}, number={4}, journal={Journal of Experimental Zoology}, publisher={Wiley}, author={Drobnis, Erma Z. and Crowe, Lois M. and Berger, Trish and Anchordoguy, Thomas J. and Overstreet, James W. and Crowe, John H.}, year={1993}, month=mar, pages={432–437} }

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