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The Role Of Vitrification In Anhydrobiosis.
J. Crowe, J. Carpenter, L. Crowe
Published 1998 · Biology, Medicine
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Numerous organisms are capable of surviving more or less complete dehydration. A common feature in their biochemistry is that they accumulate large amounts of disaccharides, the most common of which are sucrose and trehalose. Over the past 20 years, we have provided evidence that these sugars stabilize membranes and proteins in the dry state, most likely by hydrogen bonding to polar residues in the dry macromolecular assemblages. This direct interaction results in maintenance of dry proteins and membranes in a physical state similar to that seen in the presence of excess water. An alternative viewpoint has been proposed, based on the fact that both sucrose and trehalose form glasses in the dry state. It has been suggested that glass formation (vitrification) is in itself sufficient to stabilize dry biomaterials. In this review we present evidence that, although vitrification is indeed required, it is not in itself sufficient. Instead, both direct interaction and vitrification are required. Special properties have often been claimed for trehalose in this regard. In fact, trehalose has been shown by many workers to be remarkably (and sometimes uniquely) effective in stabilizing dry or frozen biomolecules, cells, and tissues. Others have not observed any such special properties. We review evidence here showing that trehalose has a remarkably high glass-transition temperature (Tg). It is not anomalous in this regard because it lies at the end of a continuum of sugars with increasing Tg. However, it is unusual in that addition of small amounts of water does not depress Tg, as in other sugars. Instead, a dihydrate crystal of trehalose forms, thereby shielding the remaining glassy trehalose from effects of the added water. Thus under less than ideal conditions such as high humidity and temperature, trehalose does indeed have special properties, which may explain the stability and longevity of anhydrobiotes that contain it. Further, it makes this sugar useful in stabilization of biomolecules of use in human welfare.
This paper references
Dehydration-induced conformational transitions in proteins and their inhibition by stabilizers.
S. Prestrelski (1993)
Is vitrification involved in depression of the phase transition temperature in dry phospholipids?
J. Crowe (1996)
Is trehalose special for preserving dry biomaterials?
L. Crowe (1996)
THE CONTROL OF EMERGENCE AND METABOLISM BY EXTERNAL OSMOTIC PRESSURE AND THE ROLE OF FREE GLYCEROL IN DEVELOPING CYSTS OF ARTEMIA SALINA.
J. Clegg (1964)
Separation of freezing- and drying-induced denaturation of lyophilized proteins using stress-specific stabilization. I. Enzyme activity and calorimetric studies.
J. Carpenter (1993)
Sugars and desiccation tolerance in seeds.
K. Koster (1988)
Formation of Glasses from Liquids and Biopolymers
C. Angell (1995)
Optimization of Lyophilization Conditions for Recombinant Human Interleukin-2 by Dried-State Conformational Analysis Using Fourier-Transform Infrared Spectroscopy
S. Prestrelski (2004)
Effects of trehalose in canine lung preservation.
T. Hirata (1994)
Phase relations and vitrification in saccharide−water solutions and the trehalose anomaly
J. Green (1989)
Successful 12-hour lung preservation with trehalose.
T. Hirata (1993)
Glass transitions in soybean seed : relevance to anhydrous biology.
Fabrizio Bruni (1991)
Germination and ion leakage are linked with phase transitions: of membrane lipids during imbibition of Typha latifolia pollen
F. Hoekstra (1992)
Infrared spectroscopic studies of lyophilization- and temperature-induced protein aggregation.
A. Dong (1995)
Low concentrations of trehalose protect isolated thylakoids against mechanical freeze-thaw damage
D. Hincha (1989)
Modes of stabilization of a protein by organic solutes during desiccation
J. F. Carpenter (1988)
Stabilization of dry membranes by mixtures of hydroxyethyl starch and glucose: the role of vitrification.
J. Crowe (1997)
Water Science Reviews 3: Water as a plasticizer: physico-chemical aspects of low-moisture polymeric systems
H. Levine (1988)
Aspects of the glass transition behaviour of mixtures of carbohydrates of low molecular weight.
P. D. Orford (1990)
The effect of sucrose and trehalose on viability of one- and two-cell rabbit embryos.
Z. Smorag (1990)
Twenty-hour canine lung preservation using newly developed solutions containing trehalose.
T. Bando (1994)
The role of trehalose and other carbohydrates in biopreservation.
Y. M. Newman (1993)
Cytoplasmic glass formation in maize embryos
F. Bruni (1992)
Stabilization of phosphofructokinase during air-drying with sugars and sugar/transition metal mixtures.
J. Carpenter (1987)
Physical factors affecting the storage stability of freeze-dried interleukin-1 receptor antagonist: glass transition and protein conformation.
B. Chang (1996)
Study of the solid-liquid state diagram of the water-glycine-sucrose system
E.Yu. Shalaev (1994)
Effects of carbohydrates on membrane stability at low water activities.
L. Crowe (1984)
Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying.
S. Leslie (1995)
Separation of freezing- and drying-induced denaturation of lyophilized proteins using stress-specific stabilization. II. Structural studies using infrared spectroscopy.
S. Prestrelski (1993)
LINKED FUNCTIONS AND RECIPROCAL EFFECTS IN HEMOGLOBIN: A SECOND LOOK.
J. Wyman (1964)
Cryoprotective Effect of Saccharides on Denaturation of Catalase by Freeze-Drying
K. Tanaka (1991)
Preservation of metabolic activity in lyophilized human erythrocytes.
R. Goodrich (1992)
Trehalose: A Cryoprotectant That Enhances Recovery and Preserves Function of Human Pancreatic Islets After Long-Term Storage
G. Beattie (1997)
Stabilization of phosphofructokinase with sugars during freeze-drying: characterization of enhanced protection in the presence of divalent cations.
J. Carpenter (1987)
The hydrophobic effect and the organization of living matter.
C. Tanford (1978)
The effects of formulation and moisture on the stability of a freeze-dried monoclonal antibody-vinca conjugate: a test of the WLF glass transition theory.
Roy Ml (1992)
Desiccation tolerance of prokaryotes.
M. Potts (1994)
Trehalose and dry dipalmitoylphosphatidylcholine revisited.
L. Crowe (1988)
Phase transitions and permeability changes in dry membranes during rehydration
J. Crowe (1989)
Glass/rubber transitions and heat capacities of binary sugar blends
Leonard X. Finegold (1989)
Biophysics and biochemistry at low temperatures
F. Franks (1985)
Anhydrobiosis: cellular adaptations to extreme dehydration.
J. Crowe (1997)
Stability of dry liposomes in sugar glasses.
W. Sun (1996)
Interactions of Stabilizers with Proteins During Freezing and Drying.
J. F. Carpenter (1995)
Trehalose inhibits ethanol effects on intact yeast cells and liposomes.
J. Mansure (1994)
An infrared spectroscopic study of the interactions of carbohydrates with dried proteins.
J. Carpenter (1989)
Do phospholipids and sucrose determine membrane phase transitions in dehydrating pollen species
F. Hoekstra (1992)
Prevention of fusion and leakage in freeze-dried liposomes by carbohydrates
L. Crowe (1986)
AN ATTEMPT TO RECOVER VIABLE HUMAN RED BLOOD CELLS AFTER FREEZE-DRYING
G. Spieles (1996)
Hydration of proteins and polypeptides.
I. Kuntz (1974)
Trehalose lowers membrane phase transitions in dry yeast cells.
S. Leslie (1994)
Preservation of structural and functional activity in lyophilized sarcoplasmic reticulum.
J. Crowe (1983)
The role of sugar, vitrification and membrane phase transition in seed desiccation tolerance
W. Sun (1994)
Glass formation and desiccation tolerance in seeds.
K. Koster (1991)
The glassy state in corn embryos.
R. Williams (1989)
Protection of freeze-dried Escherichia coli by trehalose upon exposure to environmental conditions.
E. Israeli (1993)
Effect of mannitol crystallinity on the stabilization of enzymes during freeze-drying.
K. Izutsu (1994)
Arrestment of carbohydrate metabolism during anaerobic dormancy and aerobic acidosis inArtemia embryos: determination of pH-sensitive control points
J. Carpenter (2004)
Water as ligand: preferential binding and exclusion of denaturants in protein unfolding.
S. N. Timasheff (1992)
Water and proteins. II. The location and dynamics of water in protein systems and its relation to their stability and properties.
J. Edsall (1983)
Counteracting effects of thiocyanate and sucrose on chymotrypsinogen secondary structure and aggregation during freezing, drying, and rehydration.
S. D. Allison (1996)
Glass transitions and water-food structure interactions.
L. Slade (1995)
Structure of Proteins in Lyophilized Formulations Using Fourier Transform Infrared Spectroscopy.
S. Prestrelski (1995)
Interactions between soluble sugars and POPC (1-palmitoyl-2-oleoylphosphatidylcholine) during dehydration: vitrification of sugars alters the phase behavior of the phospholipid.
K. Koster (1994)
This paper is referenced by
Glass Transition Temperatures and Fermentative Activity of Heat‐Treated Commercial Active Dry Yeasts
C. Schebor (2000)
How strongly does trehalose interact with lysozyme in the solid state? Insights from molecular dynamics simulation and inelastic neutron scattering.
A. Lerbret (2012)
Secretion of a novel developmentally regulated chitinase (family 19 glycosyl hydrolase) into the perivitelline fluid of the parasitic nematode, Ascaris suum.
J. Geng (2002)
Chapter 13 – Life Without Water: Responses of Prokaryotes to Desiccation
D. Billi (2000)
Stabilization of membranes in human platelets freeze-dried with trehalose.
J. Crowe (2003)
The preservation of liposomes by raffinose family oligosaccharides during drying is mediated by effects on fusion and lipid phase transitions.
D. Hincha (2003)
Stability of dry enzymes
M. Terebiznik (2003)
Opportunities and challenges of developing thermostable vaccines
D. Chen (2009)
Water replacement hypothesis in atomic detail--factors determining the structure of dehydrated bilayer stacks.
E. Golovina (2009)
Investigation of mycobacterial survival in non-permissive growth conditions
Asel A. Sarybaeva (2015)
Reduced protein adsorption at solid interfaces by sugar excipients
Janet R Wendorf (2004)
A rational approach to oocyte cryopreservation.
S. Paynter (2005)
A Modulating Role for Antioxidants in Desiccation Tolerance1
I. Kranner (2005)
Production of highly stable spray dried phage formulations for treatment of Pseudomonas aeruginosa lung infection
R. Y. Chang (2017)
THE DISACCHARIDE TREHALOSE INHIBITS PROINFLAMMATORY PHENOTYPE ACTIVATION IN MACROPHAGES AND PREVENTS MORTALITY IN EXPERIMENTAL SEPTIC SHOCK
L. Minutoli (2007)
Innovative technology to stabilize DNA at room temperature in tissue and cells
Steven V. Wilkinson (2010)
Isolation and characterization of a native isolate of Leuconostoc for functional attributes
P. S. Rani (2008)
Physiological changes leading to anhydrobiosis improve radiation tolerance in Polypedilum vanderplanki larvae.
M. Watanabe (2007)
Volume changes of mature human oocytes on exposure to cryoprotectant solutions used in slow cooling procedures.
S. Paynter (2005)
Preservation of Mouse Sperm by Convective Drying and Storing in 3-O-Methyl-D-Glucose
J. Liu (2012)
Potential of protein-prebiotic as protective matrices on the storage stability of vacuum-dried probiotic Lactobacillus casei
Wanticha Savedboworn (2020)
Characteristics, dynamics and mechanisms of actions of some major stress-induced biomacromolecules; addressing Artemia as an excellent biological model.
Hamidreza Khodajou-Masouleh (2020)
Simulations of Biomolecules in Electrolyte Solutions
R. Friedman (2019)
The amorphous state: first-principles derivation of the Gordon-Taylor equation for direct prediction of the glass transition temperature of mixtures; estimation of the crossover temperature of fragile glass formers; physical basis of the "Rule of 2/3".
P. Skrdla (2017)
Glass transition temperature of dried lens tissue pretreated with trehalose, maltose, or cyclic tetrasaccharide
Tetsuhiro Kawata (2014)
Polymorphism in carbohydrate self-assembly at surfaces: STM imaging and theoretical modelling of trehalose on Cu(100)
Sabine Abb (2019)
Trehalose Stabilizing Protein in a Water Replacement Scenario: Insights from Molecular Dynamics Simulation
Qiang Shao (2019)
Radiation Tolerance in Tardigrades: Current Knowledge and Potential Applications in Medicine
K. I. Jönsson (2019)
Understanding regulatory networks and engineering for enhanced drought tolerance in plants.
B. Valliyodan (2006)
Biochemistry of Anhydrobiosis in Beddingia siricidicola, a Biological Control Agent of Sirex noctilio.
M. J. Lacey (2015)
Mechanism of protein stabilization by trehalose during freeze-drying analyzed by in situ micro-raman spectroscopy.
A. Hédoux (2013)
Molecular cloning of maltooligosyltrehalose trehalohydrolase gene from Nostoc flagelliforme and trehalose-related response to stresses.
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