How Do Animals Survive Extreme Temperature Amplitudes? The Role of Natural Deep Eutectic Solvents

Recent findings have reported the reason why some living beings are able to withstand the huge thermal amplitudes between winter and summer in their natural habitats. They are able to produce metabolites decreasing deeply the crystallization temperature of water, avoiding cell disrupture due to the presence of ice crystals and overcoming osmotic effects. In vitro, the possibility to cool living cells and tissues to cryogenic temperatures in the absence of ice can be achieved through a vitrification process. Vitrification has been suggested as an alternative approach to cryopreservation and could hereafter follow an interesting biomimetic perspective. The metabolites produced by these animals are mostly sugars, organic acids, choline derivatives, or urea. When combined at a particular composition, these compounds form a new liquid phase which has been defined as Natural Deep Eutectic Solvents (NADES). In this review, we relate the findings of different areas of knowledge from evolutive biology, cryobiology...

[1]  Emma L. Smith,et al.  Deep eutectic solvents (DESs) and their applications. , 2014, Chemical reviews.

[2]  P. Villeneuve,et al.  From green chemistry to nature: The versatile role of low transition temperature mixtures. , 2016, Biochimie.

[3]  B. Luyet,et al.  Life and death at low temperatures, by B. J. Luyet ... and P. M. Gehenio ... , 1940 .

[4]  Catarina Florindo,et al.  Insights into the Synthesis and Properties of Deep Eutectic Solvents Based on Cholinium Chloride and Carboxylic Acids , 2014 .

[5]  D. Denlinger,et al.  Cryobiology of the freeze-tolerant gall fly Eurosta solidaginis:overwintering energetics and heat shock proteins , 1995 .

[6]  M. Bozorgmehr,et al.  How a protein can remain stable in a solvent with high content of urea: insights from molecular dynamics simulation of Candida antarctica lipase B in urea : choline chloride deep eutectic solvent. , 2014, Physical chemistry chemical physics : PCCP.

[7]  J. Baust,et al.  The ontogeny of cold tolerance in the gall fly, Eurosta solidagensis , 1976 .

[8]  K. Storey,et al.  Biochemical adaption for freezing tolerance in the wood frog,Rana sylvatica , 2004, Journal of Comparative Physiology B.

[9]  C. Colaco,et al.  The role of trehalose and other carbohydrates in biopreservation. , 1993, Biotechnology & genetic engineering reviews.

[10]  V. Loeschcke,et al.  Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. , 2007, Journal of insect physiology.

[11]  Gary D. Smith,et al.  Fertility Cryopreservation: Cryoprotectants , 2010 .

[12]  J. Coutinho,et al.  Enhanced Solubility of Lignin Monomeric Model Compounds and Technical Lignins in Aqueous Solutions of Deep Eutectic Solvents , 2017 .

[13]  M. Toner,et al.  Long-term storage of tissues by cryopreservation: critical issues. , 1996, Biomaterials.

[14]  I. Alnashef,et al.  Are deep eutectic solvents benign or toxic? , 2013, Chemosphere.

[15]  B. Fuller,et al.  Cryoprotectants: the essential antifreezes to protect life in the frozen state. , 2004, Cryo letters.

[16]  M. Holmstrup,et al.  Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Wesley-Smith,et al.  Intracellular ice and cell survival in cryo-exposed embryonic axes of recalcitrant seeds of Acer saccharinum: an ultrastructural study of factors affecting cell and ice structures. , 2014, Annals of botany.

[18]  B. Roelen,et al.  Cellular damage suffered by equine embryos after exposure to cryoprotectants or cryopreservation by slow-freezing or vitrification. , 2015, Equine veterinary journal.

[19]  K. Walters,et al.  Freeze tolerance in an arctic Alaska stonefly , 2009, Journal of Experimental Biology.

[20]  Jedediah K. Lewis,et al.  The Grand Challenges of Organ Banking: Proceedings from the first global summit on complex tissue cryopreservation. , 2016, Cryobiology.

[21]  G. Fahy,et al.  Principles of cryopreservation by vitrification. , 2015, Methods in molecular biology.

[22]  D. Lenoir,et al.  Low melting sugar–urea–salt mixtures as solvents for organic reactions—estimation of polarity and use in catalysis , 2006 .

[23]  B. Luyet,et al.  Electron microscope study of erythrocytes in rapidly cooled suspensions containing various concentrations of glycerol. , 1968, Biodynamica.

[24]  Marina Cvjetko Bubalo,et al.  Evaluation of toxicity and biodegradability of choline chloride based deep eutectic solvents. , 2015, Ecotoxicology and environmental safety.

[25]  Y. Choi,et al.  Tailoring properties of natural deep eutectic solvents with water to facilitate their applications. , 2015, Food chemistry.

[26]  B. König,et al.  Low-melting sugar-urea-salt mixtures as solvents for Diels-Alder reactions. , 2005, Chemical communications.

[27]  A. E. Oliver,et al.  The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state. , 2001, Cryobiology.

[28]  R. Lee,et al.  Cryoprotectants and Extreme Freeze Tolerance in a Subarctic Population of the Wood Frog , 2015, PloS one.

[29]  A. S. Parkes,et al.  Revival of Spermatozoa after Vitrification and Dehydration at Low Temperatures , 1949, Nature.

[30]  G. J. Morris,et al.  Controlled ice nucleation in cryopreservation--a review. , 2013, Cryobiology.

[31]  B. Wowk.  Thermodynamic aspects of vitrification. , 2010, Cryobiology.

[32]  M. E. Clark,et al.  Living with water stress: evolution of osmolyte systems. , 1982, Science.

[33]  A. Elbein,et al.  New insights on trehalose: a multifunctional molecule. , 2003, Glycobiology.

[34]  Geert-Jan Witkamp,et al.  Ionic liquids and deep eutectic solvents in natural products research: mixtures of solids as extraction solvents. , 2013, Journal of natural products.

[35]  L. Sømme,et al.  Cold tolerance in Tardigrada from Dronning Maud Land, Antarctica , 1995, Polar Biology.

[36]  J. Zelený,et al.  Multiple component system of sugars and polyols in the overwintering spruce bark beetle, Ips typographus. , 2007, Journal of insect physiology.

[37]  Jonathan C. Wright.  Cryptobiosis 300 years on from van Leuwenhoek : what have we learned about tardigrades? , 2001 .

[38]  S. Kalhan,et al.  Glyceroneogenesis and the Source of Glycerol for Hepatic Triacylglycerol Synthesis in Humans* , 2001, The Journal of Biological Chemistry.

[39]  M. Hayyan,et al.  Natural deep eutectic solvents: cytotoxic profile , 2016, SpringerPlus.

[40]  G. Fahy,et al.  Deep supercooling, vitrification and limited survival to –100°C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae , 2010, Journal of Experimental Biology.

[41]  V. Košťál,et al.  Physiological and biochemical analysis of overwintering and cold tolerance in two Central European populations of the spruce bark beetle, Ips typographus. , 2011, Journal of insect physiology.

[42]  Yonggyun Kim,et al.  Trehalose, a Major Sugar Cryoprotectant of the Overwintering Rice Water Weevil, Lissorhoptrus oryzophilus (Coleoptera: Curculionidae) , 2002 .

[43]  R. Lee,et al.  Enzymatic Regulation of Glycogenolysis in a Subarctic Population of the Wood Frog: Implications for Extreme Freeze Tolerance , 2013, PloS one.

[44]  I. Arends,et al.  Are Natural Deep Eutectic Solvents the Missing Link in Understanding Cellular Metabolism and Physiology?[W] , 2011, Plant Physiology.

[45]  R. Lee,et al.  Cryoprotection by urea in a terrestrially hibernating frog , 2005, Journal of Experimental Biology.

[46]  G. M. Fahy,et al.  Ice-free cryopreservation of mouse embryos at −196 °C by vitrification , 1985, Nature.

[47]  V. Košťál,et al.  Overwintering Strategy and Mechanisms of Cold Tolerance in the Codling Moth (Cydia pomonella) , 2013, PloS one.

[48]  Steffen Hengherr,et al.  Trehalose and anhydrobiosis in tardigrades – evidence for divergence in responses to dehydration , 2008, The FEBS journal.

[49]  F. Peña,et al.  Toxicity of glycerol for the stallion spermatozoa: effects on membrane integrity and cytoskeleton, lipid peroxidation and mitochondrial membrane potential. , 2012, Theriogenology.

[50]  D. Renault,et al.  Cold exposure and associated metabolic changes in adult tropical beetles exposed to fluctuating thermal regimes , 2007, The FEBS journal.

[51]  V. Košťál,et al.  Dynamics of cold hardiness, supercooling and cryoprotectants in diapausing and non-diapausing pupae of the cabbage root fly, Delia radicum L. , 1995 .

[52]  R. Reis,et al.  Properties and thermal behavior of natural deep eutectic solvents , 2016 .

[53]  Geert-Jan Witkamp,et al.  Natural deep eutectic solvents as new potential media for green technology. , 2013, Analytica chimica acta.

[54]  D W Hutmacher,et al.  Vitrification as a prospect for cryopreservation of tissue-engineered constructs. , 2007, Biomaterials.

[55]  N. Desai,et al.  Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis. , 2010, Reproductive biomedicine online.

[56]  D. Denlinger,et al.  Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica , 2007, Journal of Experimental Biology.

[57]  Peter Westh,et al.  Trehalose accumulation in the tardigrade Adorybiotus coronifer during anhydrobiosis , 1991 .

[58]  J. Buitink,et al.  Intracellular glasses and seed survival in the dry state. , 2008, Comptes rendus biologies.

[59]  Rui L. Reis,et al.  Natural Deep Eutectic Solvents – Solvents for the 21st Century , 2014 .

[60]  M. Holmstrup,et al.  Freeze tolerance in Aporrectodea caliginosa and other earthworms from Finland. , 2007, Cryobiology.

[61]  P. Westh,et al.  Survival of the Cryptobiotic Eutardigrade Adorybiotus coronifer during cooling to -196°C: Effect of Cooling Rate, Trehalose Level, and Short-Term Acclimation , 1992 .

[62]  I. Roy,et al.  Effect of trehalose on protein structure , 2008, Protein science : a publication of the Protein Society.

[63]  H. Vaudry,et al.  Freeze tolerance in the wood frog Rana sylvatica is associated with unusual structural features in insulin but not in glucagon. , 1998, Journal of molecular endocrinology.

[64]  K L Koster,et al.  Glass formation and desiccation tolerance in seeds. , 1991, Plant physiology.

[65]  B. Ata,et al.  A randomized controlled study of human Day 3 embryo cryopreservation by slow freezing or vitrification: vitrification is associated with higher survival, metabolism and blastocyst formation. , 2008, Human reproduction.

[66]  A. Molina-García,et al.  Glass transition and heat capacity behaviors of plant vitrification solutions , 2014 .

[67]  M. C. Kroon,et al.  Low-transition-temperature mixtures (LTTMs): a new generation of designer solvents. , 2013, Angewandte Chemie.

[68]  D. Pegg.  Principles of cryopreservation. , 2007, Methods in molecular biology.

[69]  Minke Tang,et al.  Stabilization of Dry Mammalian Cells: Lessons from Nature1 , 2005, Integrative and comparative biology.

[70]  N. Nielsen,et al.  Freeze tolerance and accumulation of cryoprotectants in the enchytraeid Enchytraeus albidus (Oligochaeta) from Greenland and Europe. , 2008, Cryobiology.