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Methods for dehydration-tolerance: Depression of the phase transition temperature in dry membranes and carbohydrate vitrification

Published online by Cambridge University Press:  19 September 2008

Ann E. Oliver*
Affiliation:
Section of Molecular and Cellular Biology, University of California, Davis, CA 95616, USA
Lois M. Crowe
Affiliation:
Section of Molecular and Cellular Biology, University of California, Davis, CA 95616, USA
John H. Crowe
Affiliation:
Section of Molecular and Cellular Biology, University of California, Davis, CA 95616, USA
*
*+1 530 752 5305[email protected]

Abstract

Anhydrobiosis, or life without water, is the remarkable ability of certain types of plants and animals to survive almost total dehydration. This phenomenon requires a coordinated series of events within the cells of anhydrobiotes that protect their cellular components, particularly proteins and lipid membranes, from damage caused by the removal of water. Much of what is now understood about preserving biological samples during drying was learned by studying naturally desiccation-tolerant organisms and extended using model systems such as phospholipid vesicles. Most anhydrobiotic organisms accumulate disaccharides in their cells and tissues during the dehydration process. These carbohydrates, usually sucrose or trehalose, satisfy two criteria that appear to be necessary for protecting membranes during desiccation and during storage in the dry state. These requirements include: (1) depression of the gel-to-liquid crystalline phase transition temperature (Tm) in the dehydrated lipid to a temperature at or near that of the hydrated lipid, a process that appears to require a direct interaction between the carbohydrates and the lipid molecules of the membrane; and (2) formation of a carbohydrate glass with a relatively high glass transition temperature, leading to inhibition of fusion between the vesicles.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 1998

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References

Angell, C A, Bressel, R D, Green, J L, Kanno, H, Oguni, M and Sare, E J (1994) Liquid fragility and the glass transition in water and aqueous solutions. Journal of Food Engineering 22, 115142.CrossRefGoogle Scholar
Bruni, F and Leopold, A C (1991) Glass transitions in soybean seed. Plant Physiology 96, 660663.CrossRefGoogle ScholarPubMed
Bruni, F and Leopold, A C (1992) Cytoplasmic glass formation in maize embryos. Seed Science Research 2, 251253.CrossRefGoogle Scholar
Bryant, G and Wolfe, J (1992) Interfacial forces in cryobiology and anhydrobiology. Cryo-Letters 13, 2336.Google Scholar
Caffrey, M, Fonseca, V and Leopold, C A (1988) Lipid-sugar interactions. Plant Physiology 86, 754758.CrossRefGoogle ScholarPubMed
Carpenter, J F and Chang, B S (1996) Lyophilization of protein pharmaceuticals. pp. 199263in Avis, K,Wu, V, (Eds). Biotechnology and biopharmaceutical manufacturing, processing and preservation. Buffalo Grove, IL, Intepharm Press.Google Scholar
Clerc, S G and Thompson, T E (1995) Permeability of dimyristoyl phosphatidylcholine/dipalmitoyl phosphatidlycholine bilayer membranes with coexisting gel and liquid-crystalline phases. Biophysical Journal 68, 23332341.CrossRefGoogle Scholar
Crowe, J H and Clegg, J S (1973) Anhydrobiosis. Stroudsburg, PA, Dowden, Hutchinson and Ross, Inc.Google Scholar
Crowe, J H and Crowe, L M (1992) Preservation of liposomes by freeze drying. in Gregoriadis, G (Ed.). Liposome technology. (2nd edition) Boca Raton, FL, CRC Press.Google Scholar
Crowe, L M and Crowe, J H (1988) Trehalose and dry dipalmitoylphosphatidylcholine revisited. Biochimica et Biophysica Acta 946, 193201.CrossRefGoogle ScholarPubMed
Crowe, L M and Crowe, J H (1995) Freeze-dried liposomes. pp. 237272in Peuisieux, F, Couvreur, P, Delattre, J,Devissaguet, J-P. (Eds) Liposomes, new systems and new trends in their applications. Paris, Editions de Sante.Google Scholar
Crowe, J H, Crowe, L M and Chapman, D (1984a) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223, 701703.CrossRefGoogle ScholarPubMed
Crowe, J H, Crowe, L M and Chapman, D (1984b) Infrared spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Archives of Biochemistry and Biophysics 232, 400407.CrossRefGoogle ScholarPubMed
Crowe, L M, Womersley, C, Crowe, J H, Reid, D, Appel, L and Rudolph, A (1986) Prevention of fusion and leakage in freeze-dried liposomes by carbohydrates. Biochimica et Biophysica Acta 861, 131140.CrossRefGoogle Scholar
Crowe, J H, Crowe, L M and Hoekstra, F A (1989a) Phase transitions and permeability changes in dry membranes during rehydration. Mini review. Journal of Bioenergetics and Biomembranes 21, 7791.CrossRefGoogle Scholar
Crowe, J H, Hoekstra, F A and Crowe, L M (1989b) Membrane phase transitions are responsible for imbibitional damage in dry pollen. Proceedings of the National Academy of Sciences, USA 86, 520523.CrossRefGoogle ScholarPubMed
Crowe, J H, Hoekstra, F A, Crowe, L M, Anchordoguy, T J and Drobnis, E (1989c) Lipid phase transitions measured in intact cells with Fourier transform infrared spectroscopy. Cryobiology 26, 7684.CrossRefGoogle ScholarPubMed
Crowe, J H, Leslie, S B and Crowe, L M (1994) Is vitrification sufficient to preserve liposomes during freeze-drying? Cryobiology 31, 355366.CrossRefGoogle ScholarPubMed
Crowe, J H, Hoekstra, F A, Nguyen, K H N and Crowe, L M (1996a) Is vitrification involved in depression of the phase transition temperature in dry phospholipids? Biochimica et Biophysica Acta 1280, 187196.CrossRefGoogle ScholarPubMed
Crowe, L M, Reid, D S and Crowe, J H (1996b) Is trehalose special for preserving dry biomaterials? Biophysical Journal 71, 20872093, 1996.Google Scholar
Crowe, J H, Crowe, L M, Carpenter, J F, Prestrelski, S, Hoekstra, F A, de Araujo, P and Panek, A D (1997a) Anhydrobiosis: cellular adaptation to extreme dehydration. pp. 14451477in Dantzler, W H (Ed). Handbook of physiology. (Vol. II) Oxford, Oxford University Press.Google Scholar
Crowe, J H, Carpenter, J F and Crowe, L M (1997b) The role of vitrification in anhydrobiosis. Annual Review of Physiology 60, 73103.CrossRefGoogle Scholar
Crowe, J H, Oliver, A E, Hoekstra, F A and Crowe, L M (1997c) Stabilization of dry membranes by mixtures of hydroxyethyl starch and glucose: the role of vitrification. Cryobiology 35, 2030.CrossRefGoogle ScholarPubMed
Dickie, J B, Ellis, R H, Kraak, H L, Ryder, K and Tompsett, P B (1990) Temperature and seed storage longevity. Annals of Botany 65, 197204.CrossRefGoogle Scholar
Ding, S.-P., Fan, J, Green, J L, Lu, Q, Sanchez, E and Angell, C A (1996) Vitrification of trehalose by water loss from its crystalline dihydrate. Journal of Thermal Analysis 47, 13911405.CrossRefGoogle Scholar
Drennan, P M, Smith, M T, Goldsworthy, D and van Staden, J (1993) The occurrence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius Welw. Journal of Plant Physiology 142, 493496.CrossRefGoogle Scholar
Ellis, R H, Osei-Bonsu, K and Roberts, E H (1982) The influence of genotype, temperature and moisture on seed longevity in chickpea, cowpea, and soya bean. Annals of Botany 50, 6982.CrossRefGoogle Scholar
Ellis, R H and Roberts, E H (1980) Improved equations for the prediction of seed longevity. Annals of Botany 45, 1330.CrossRefGoogle Scholar
Finegold, L, Franks, F and Hatley, R H M (1990) Glass/rubber transitions and heat capacities of binary sugar blends. Journal of the Chemical Society. Faraday Transactions 85, 29452951.CrossRefGoogle Scholar
Franks, F (1985) Biophysics and biochemistry at low temperatures. Cambridge, UK, Cambridge Press.Google Scholar
Gadd, G M, Chalmers, K and Reed, R H (1987) The role of trehalose in dehydration resistance of Saccharomyces cerevisiae. FEMS Microbiology Letters 48, 249254.CrossRefGoogle Scholar
Green, J L and Angell, C A (1989) Phase relations and vitrification in saccharide-water solutions and the trehalose anomaly. Journal of Physical Chemistry 93, 28802882.CrossRefGoogle Scholar
Harrigan, P R, Madden, T D and Cullis, P R (1990) Protection of liposomes during dehydration or freezing. Chemistry and Physics of Lipids 52, 139149.CrossRefGoogle ScholarPubMed
Hoekstra, F A (1986) Water content in relation to stress in pollen. pp. 102122in Leopold, A C (Ed.) Membranes, metabolism and dry organisms. Ithaca, NY, Comstock Pub. Assoc.Google Scholar
Hoekstra, F A, Crowe, J H and Crowe, L M (1992a) Germination and ion leakage are linked with phase transitions of membrane lipids during imbibition of Typha latifolia pollen. Physiologia Plantarum 84, 2934.CrossRefGoogle Scholar
Hoekstra, F A, Crowe, J H, Crowe, L M, van Roekel, T and Vermeer, E (1992b) Do phospholipids and sucrose determine membrane phase transitions in dehydrating pollen species? Plant, Cell and Environment 15, 601606.CrossRefGoogle Scholar
Ingram, J and Bartels, D (1996) The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 377403.CrossRefGoogle ScholarPubMed
Koster, K L and Leopold, A C (1988) Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829832.CrossRefGoogle ScholarPubMed
Koster, K L, Webb, M S, Bryant, G and Lynch, D V (1994) Interactions between soluble sugars and POPC during dehydration: vitrification of sugars alters the phase behavior of the phospholipid. Biochimica et Biophysica Acta 1193, 143150.CrossRefGoogle ScholarPubMed
Leprince, O and Walters-Vertucci, C (1995) A calorimetric study of the glass transition behaviors in axes of bean seeds with relevance to storage stability. Plant Physiology 109, 14711481.CrossRefGoogle ScholarPubMed
Leslie, S B, Israeli, E, Lighthart, B, Crowe, J H and Crowe, L M (1995) Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Applied and Environmental Microbiology 61, 35923597.CrossRefGoogle ScholarPubMed
Leslie, S B, Teter, S A, Crowe, L M and Crowe, J H (1994) Trehalose lowers membrane phase transitions in dry yeast cells. Biochimica et Biophysica Acta 1192, 713.CrossRefGoogle ScholarPubMed
Levine, H and Slade, L (1988) Water as a plasticizer: physico-chemical aspects of low-moisture polymeric systems, pp. 79185in Franks, F (Ed.) Water science reviews. (Vol. 3) Cambridge, UK, Cambridge Press.CrossRefGoogle Scholar
Loomis, S H, Madin, K A D and Crowe, J H (1980a) Anhydrobiosis in nematodes: biosynthesis of trehalose. Journal of Experimental Zoology 211, 311320.CrossRefGoogle Scholar
Loomis, S H, O'Dell, S J and Crowe, J H (1980b) Anhydrobiosis in nematodes: control of the synthesis of trehalose during induction. Journal of Experimental Zoology 211, 321330.CrossRefGoogle Scholar
Orford, P D, Parker, R and Ring, S G (1990) Aspects of glass transition behavior of mixtures of carbohydrates of low molecular weight. Carbohydrate Research 196, 1118.CrossRefGoogle ScholarPubMed
Potts, M (1994) Desiccation tolerance of prokaryotes. Microbiological Reviews 58, 755805.CrossRefGoogle ScholarPubMed
Roos, Y (1993) Melting and glass transitions of low molecular weight carbohydrates. Carbohydrate Research 238, 3948.CrossRefGoogle Scholar
Roos, Y and Karel, M (1991) Water and molecular weight effects on glass transitions in amorphous carbohydrates and carbohydrate solutions. Journal of Food Science 56, 16761681.CrossRefGoogle Scholar
Slade, L and Levine, H (1991) Beyond water activity: recent advances based on an alternative approach to the assessment of food quality and safety. Critical Reviews of Food Science and Nutrition 30, 115360.CrossRefGoogle Scholar
Slade, L and Levine, H (1995) Glass transitions and water-food structure interactions. pp. 103269in Kinsella, J E (Ed.) Advances in food and nutrition research. (Vol. 38) San Diego, Academic Press.Google Scholar
Sun, W Q and Leopold, A C (1994) Glassy state and seed storage stability: a viability equation analysis. Annals of Botany 74, 601604.CrossRefGoogle Scholar
Sun, W Q and Leopold, A C (1997) Cytoplasmic vitrification and survival of anhydrobiotic organisms. Comparative Biochemical Physiology 117A, 327333.CrossRefGoogle Scholar
Sun, W Q, Leopold, A C, Crowe, L M and Crowe, J H (1996) Stability of dry liposomes in sugar glasses. Biophysical Journal 70, 17691776.CrossRefGoogle ScholarPubMed
Tsvetkov, T D, Tsonev, L I, Tsvetkova, N M, Koynova, R D and Tenchov, B G (1989) Effect of trehalose on the phase properties of hydrated and lyophilized dipalmitoylphosphatidylcholine multilayers. Cryobiology 26, 162169.CrossRefGoogle ScholarPubMed
Tsvetkova, N M, Tenchov, B, Tsonev, L and Tsvetkov, Ts (1988) Dependence of trehalose protective action on the initial phase state of dipalmitoylphosphatidylcholine bilayers. Cryobiology 25, 256263.CrossRefGoogle ScholarPubMed
Williams, R J and Leopold, A C (1989) The glassy state in corn embryos. Plant Physiology 89, 977981.CrossRefGoogle Scholar
Womersley, C, Uster, P S, Rudolph, A S and Crowe, J H (1986) Inhibition of dehydration-induced fusion between liposomal membranes by carbohydrates as measured by fluorescence energy transfer. Cryobiology 23, 245255.CrossRefGoogle ScholarPubMed