Abstract
This chapter describes the consequences of cold exposure and ice formation on both the cellular, tissue and the organismal level in cold tolerant ectothermic organisms. This includes the direct implication of cold “per se” on various parameters such as pH, membrane fluidity and phase transitions, ionic gradients, metabolism, cold denaturation of proteins, ice nucleation, ice growth, freezing-induced cellular dehydration, the role of aquaporins and the mechanical stress caused by ice, while referring to the different aspects described in the previous chapter on ice in general. Defensive/preventive adaptations and mechanisms of the organisms are described as well, along with a description of freeze tolerance and freeze avoidance. The synthesis and mechanisms of action of low molecular weight cryoprotectants as well as their distribution are discussed. High molecular weight cryoprotectants are also described concluding with the introduction of the AFPs.
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References
Alejevski F (2012) Seasonal transcription of antifreeze protein genes in larvae of Rhagium mordax and its expression in Drosophila melanogaster. M.Sc. Thesis. Department of Science and Environment, Roskilde University
Andersen HD, Wang C, Arleth L, Peters GH, Westh P (2011) Reconciliation of opposing views on membrane-sugar interactions. Proc Natl Acad Sci U S A 108:1874–1878
Angell CA (1982) Supercooled water. In: Franks F (ed) Water and aqueous solutions at subzero temperatures. Springer, Boston, MA, pp 1–81
Angell CA (1983) Supercooled water. Annu Rev Phys Chem 34:593–630
Anishkin A, Loukin SH, Teng J, Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc Natl Acad Sci U S A 111:7898–7905
Ansart A, Vernon P (2003) Cold hardiness in molluscs. Acta Oecol 24:95–102
Avanti C, Saluja V, van Streun EL, Frijlink HW, Hinrichs WL (2014) Stability of lysozyme in aqueous extremolyte solutions during heat shock and accelerated thermal conditions. PLoS One 9:e86244
Bahrndorff S, Tunnacliffe A, Wise MJ, McGee B, Holmstrup M, Loeschcke V (2009) Bioinformatics and protein expression analyses implicate LEA proteins in the drought response of Collembola. J Insect Physiol 55:210–217
Bayley JS, Winther CB, Andersen MK, Gronkjaer C, Nielsen OB, Pedersen TH, Overgaard J (2018) Cold exposure causes cell death by depolarization-mediated Ca(2+) overload in a chill-susceptible insect. Proc Natl Acad Sci U S A 115:E9737–E9744
Ben-Naim A (2013) Theory of cold denaturation of proteins. Adv Biol Chem 3:11
Bennett VA, Sformo T, Walters K, Toien O, Jeannet K, Hochstrasser R, Pan Q, Serianni AS, Barnes BM, Duman JG (2005) Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): roles of antifreeze proteins, polyols, dehydration and diapause. J Exp Biol 208:4467–4477
Berman DI, Meshcheryakova EN, Bulakhova NA (2016) Extreme negative temperatures and body mass loss in the Siberian salamander (Salamandrella keyserlingii, amphibia, hynobiidae). Dokl Biol Sci 468:137–141
Bigg EK (1953) The supercooling of water. Proc Phys Soc Sect B 66:688–694
Bredow M, Walker VK (2017) Ice-binding proteins in plants. Front Plant Sci 8:2153–2153
Brown DJ, Sönnichsen FD (2002) The structure of fish antifreeze proteins. In: Fish antifreeze proteins, vol 1. World Scientific, River Edge, NJ, pp 109–138
Calderon S, Holmstrup M, Westh P, Overgaard J (2009) Dual roles of glucose in the freeze-tolerant earthworm Dendrobaena octaedra: cryoprotection and fuel for metabolism. J Exp Biol 212:859–866
Cannon RJC, Block W (1988) Cold tolerance of microarthropods. Biol Rev 63:23–77
Cheng CC, DeVries AL (1991) The role of antifreeze glycopeptides and peptides in the freezing avoidance of cold-water fish. In: di Prisco G (ed) Life under extreme conditions. Springer, Berlin, pp 1–14
Cheng CCM, DeVries AL (2002) Origins and evolution of fish antifreeze proteins. In: Fish antifreeze proteins, vol 1. World Scientific, River Edge, NJ, pp 83–107
Clerc SG, Thompson TE (1995) Permeability of dimyristoyl phosphatidylcholine/dipalmitoyl phosphatidylcholine bilayer membranes with coexisting gel and liquid-crystalline phases. Biophys J 68:2333–2341
Cossins AR, Murray PA, Gracey AY, Logue J, Polley S, Caddick M, Brooks S, Postle T, Maclean N (2002) The role of desaturases in cold-induced lipid restructuring. Biochem Soc Trans 30:1082–1086
Costanzo JP, Claussen DL (1990) Natural freeze tolerance in the terrestrial turtle, Terrapene carolina. J Exp Zool 254:228–232
Costanzo JP, Lee RE Jr (1995) Supercooling and ice nucleation in vertebrate ectotherms. APS Press, St. Paul, pp 221–237
Costanzo JP, Lee RE Jr (2013) Avoidance and tolerance of freezing in ectothermic vertebrates. J Exp Biol 216:1961–1967
Costanzo JP, Wright MF, Lee RE (1992) Freeze tolerance as an overwintering adaptation in Cope’s grey treefrog (Hyla chrysoscelis). J Exp Zool 283(3):221–225
Crowe JH, Crowe LM, Chapman D (1984a) Infrared spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Arch Biochem Biophys 232:400–407
Crowe JH, Whittam MA, Chapman D, Crowe LM (1984b) Interactions of phospholipid monolayers with carbohydrates. Biochim Biophys Acta 769:151–159
DeVries AL, Wohlschlag DE (1969) Freezing resistance in some Antarctic fishes. Science 163:1073–1075
Doelling AR, Griffis N, Williams JB (2014) Repeated freezing induces oxidative stress and reduces survival in the freeze-tolerant goldenrod gall fly, Eurosta solidaginis. J Insect Physiol 67:20–27
Duman JG (1977) The role of macromolecular antifreeze in the darkling beetle, Meracantha contracta. J Comp Physiol 115:279–286
Duman JG (1980) Factors involved in overwintering survival of the freeze tolerant beetle, Dendroides canadensis. J Comp Physiol 136:52–59
Duman JG (1982) Insect antifreezes and ice-nucleating agents. Cryobiology 19:613–627
Duman JG (2002) The inhibition of ice nucleators by insect antifreeze proteins is enhanced by glycerol and citrate. J Comp Physiol B 172:163–168
Duman JG, Devries AL (1974) Freezing resistance in winter flounder Pseudopleuronectes americanus. Nature 247:237–238
Duman J, Horwath K (1983) The role of hemolymph proteins in the cold tolerance of insects. Annu Rev Physiol 45:261–270
Duman JG, Olsen MT (1993) Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30:322–328
Duman JG, Patterson JL, Kozak JJ, DeVries AL (1980) Isopiestic determination of water binding by fish antifreeze glycoproteins. Biochim Biophys Acta 626:332–336
Duman JG, Neven LG, Beals JM, Olson KR, Castellino FJ (1985) Freeze-tolerance adaptations, including haemolymph protein and lipoprotein nucleators, in the larvae of the cranefly Tipula trivittata. J Insect Physiol 31:1–8
Duman JG, Wu DW, Xu L, Tursman D, Olsen MT (1991) Adaptations of insects to subzero temperatures. Q Rev Biol 66:387–410
Duman JG, Olsen TM, Yeung KL, Jerva F (1995) The roles of ice nucleators in cold tolerant invertebrates. APS Press, St. Paul, pp 201–219
Duman JG, Bennett V, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266
Eastman JT (1993) 11 - Antifreeze Glycopeptides. In: Eastman JT (ed) Antarctic fish biology. Academic Press, San Diego, pp 178–201
Elnitsky MA, Lee RE (2009) The rapid cold-hardening response in insects: ecological significance and physiological mechanisms. J Exp Biol 216:3937–3945
Finn RN, Cerda J (2015) Evolution and functional diversity of aquaporins. Biol Bull 229:6–23
Fisker KV, Overgaard J, Sorensen JG, Slotsbo S, Holmstrup M (2014) Roles of carbohydrate reserves for local adaptation to low temperatures in the freeze tolerant oligochaete Enchytraeus albidus. J Comp Physiol B 184:167–177
Franks F (1985) Biophysics and biochemistry at low temperatures. Cambridge University Press, Cambridge [Cambridgeshire]
Franks F, Mathias SF, Hatley RH (1990) Water, temperature and life. Philos Trans R Soc Lond Ser B Biol Sci 326:517–531. discussion 531–533
Garlick KM, Robertson RM (2007) Cytoskeletal stability and heat shock-mediated thermoprotection of central pattern generation in Locusta migratoria. Comp Biochem Physiol A Mol Integr Physiol 147:344–348
Gehrken U (1984) Winter survival of an adult bark beetle Ips acuminatus Gyll. J Insect Physiol 30:421–429
Gehrken U (1992) Inoculative freezing and thermal hysteresis in the adult beetles Ips acuminatus and Rhagium inquisitor. J Insect Physiol 38:519–524
Gehrken U, Strømme A, Lundheim R, Zachariassen KE (1991) Inoculative freezing in overwintering tenebrionid beetle, Bolitophagus reticulatus Panz. J Insect Physiol 37:683–687
Gekko K, Timasheff SN (1981a) Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures. Biochemistry 20:4667–4676
Gekko K, Timasheff SN (1981b) Thermodynamic and kinetic examination of protein stabilization by glycerol. Biochemistry 20:4677–4686
Gilbert JA, Davies PL, Laybourn-Parry J (2005) A hyperactive, Ca2+-dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiol Lett 245:67–72
Goldstein DL, Frisbie J, Diller A, Pandey RN, Krane CM (2010) Glycerol uptake by erythrocytes from warm- and cold-acclimated Cope’s gray treefrogs. J Comp Physiol B Biochem Syst Environ Physiol 180:1257–1265
Goto SG, Philip BN, Teets NM, Kawarasaki Y, Lee RE Jr, Denlinger DL (2011) Functional characterization of an aquaporin in the Antarctic midge Belgica antarctica. J Insect Physiol 57:1106–1114
Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405
Griffith M, Ala P, Yang DS, Hon WC, Moffatt BA (1992) Antifreeze protein produced endogenously in winter rye leaves. Plant Physiol 100:593–596
Hartley LM, Packard MJ, Packard GC (2000) Accumulation of lactate by supercooled hatchlings of the painted turtle (Chrysemys picta): implications for overwinter survival. J Comp Physiol B 170:45–50
Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42
Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227
Hazel JR, McKinley SJ, Williams EE (1992) Thermal adaptation in biological membranes: interacting effects of temperature and pH. J Comp Physiol B 162:593–601
Hoback WW, Stanley DW (2001) Insects in hypoxia. J Insect Physiol 47:533–542
Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, New Jersey
Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, Oxford, New York
Holmstrup M (2014) The ins and outs of water dynamics in cold tolerant soil invertebrates. J Therm Biol 45:117–123
Holmstrup M, Westh P (1994) Dehydration of earthworm cocoons exposed to cold - a novel cold-hardiness mechanism. J Comp Physiol B 164:312–315
Holmstrup M, Costanzo JP, Lee RE (1999) Cryoprotective and osmotic responses to cold acclimation and freezing in freeze-tolerant and freeze-intolerant earthworms. J Comp Physiol B 169:207–214
Holmstrup M, Bayley M, Ramlov H (2002) Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates. Proc Natl Acad Sci U S A 99:5716–5720
Hoshino T, Kiriaki M, Ohgiya S, Fujiwara M, Kondo H, Nishimiya Y, Yumoto I, Tsuda S (2003) Antifreeze proteins from snow mold fungi. Can J Bot 81:1175–1181
Hub JS, de Groot BL (2008) Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc Natl Acad Sci U S A 105:1198–1203
Irwin JT, Lee RE (2000) Mild winter temperatures reduce survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). J Insect Physiol 46:655–661
Irwin JT, Lee JRE (2003) Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100:71–78
Izumi Y, Sonoda S, Yoshida H, Danks HV, Tsumuki H (2006) Role of membrane transport of water and glycerol in the freeze tolerance of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae). J Insect Physiol 52:215–220
Izumi Y, Sonoda S, Tsumuki H (2007) Effects of diapause and cold-acclimation on the avoidance of freezing injury in fat body tissue of the rice stem borer, Chilo suppressalis Walker. J Insect Physiol 53:685–690
Joanisse DR, Storey KB (1996) Oxidative damage and antioxidants in Rana sylvatica, the freeze-tolerant wood frog. Am J Phys 271:R545–R553
Kawarasaki Y, Teets NM, Denlinger DL, Lee RE Jr (2013) The protective effect of rapid cold-hardening develops more quickly in frozen versus supercooled larvae of the Antarctic midge, Belgica antarctica. J Exp Biol 216:3937–3945
Kent B, Hunt T, Darwish TA, Hauss T, Garvey CJ, Bryant G (2014) Localization of trehalose in partially hydrated DOPC bilayers: insights into cryoprotective mechanisms. J R Soc Interface 11:20140069
Kikawada T, Saito A, Kanamori Y, Nakahara Y, Iwata K, Tanaka D, Watanabe M, Okuda T (2007) Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells. Proc Natl Acad Sci U S A 104:11585–11590
Kim M, Robich RM, Rinehart JP, Denlinger DL (2006) Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens. J Insect Physiol 52:1226–1233
King PA, Rosholt MN, Storey KB (1993) Adaptations of plasma membrane glucose transport facilitate cryoprotectant distribution in freeze-tolerant frogs. Am J Phys 265:R1036–R1042
King PA, Rosholt MN, Storey KB (1995) Seasonal changes in plasma membrane glucose transporters enhance cryoprotectant distribution in the freeze-tolerant wood frog. Can J Zool 73:1–9
Knight CA, Wen D, Laursen RA (1995) Nonequilibrium antifreeze peptides and the recrystallization of ice. Cryobiology 32:23–34
Kostál V, Tamura M, Borovanska M, Zahradníčková H (2004) Enzymatic capacity for accumulation of polyol cryoprotectants changes during diapause development in the adult red firebug, Pyrrhocoris apterus. Physiol Entomol 29(4):344–355
Kristiansen E, Zachariassen KE (2001) Effect of freezing on the transmembrane distribution of ions in freeze-tolerant larvae of the wood fly Xylophagus cinctus (Diptera, Xylophagidae). J Insect Physiol 47:585–592
Kristiansen E, Ramlov H, Hojrup P, Pedersen SA, Hagen L, Zachariassen KE (2011) Structural characteristics of a novel antifreeze protein from the longhorn beetle Rhagium inquisitor. Insect Biochem Mol Biol 41:109–117
Kristiansen E, Wilkens C, Vincents B, Friis D, Lorentzen AB, Jenssen H, Lobner-Olesen A, Ramlov H (2012) Hyperactive antifreeze proteins from longhorn beetles: some structural insights. J Insect Physiol 58:1502–1510
Krog JO, Zachariassen KE, Larsen B, Smidsrød O (1979) Thermal buffering in afro-alpine plants due to nucleating agent-induced water freezing. Nature 282:300–301
Lange R, Staaland H, Mostad A (1972) The effect of salinity and temperature on solubility of oxygen and respiratory rate in oxygen-dependent marine invertebrates. J Exp Mar Biol Ecol 9:217–229
Layne JR Jr, Jones AL (2001) Freeze tolerance in the gray treefrog: cryoprotectant mobilization and organ dehydration. J Exp Zool 290:1–5
Layne JR Jr, Lee RE Jr (1987) Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Can J Zool 65:2062–2065
Layne JR Jr, Lee RE Jr (1989) Seasonal variation in freeze tolerance and ice content of the tree frog Hyla versicolor. J Exp Zool 249:133–137
Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta 1666:62–87
Lee RE, Denlinger DL (2010) Rapid cold-hardening: ecological significance and underpinning mechanisms. In: Denlinger DL, Lee JRE (eds) Low temperature biology of insects. Cambridge University Press, Cambridge, pp 35–58
Lee RE, Chen C-P, Denlinger DL (1987) A rapid cold-hardening process in insects. Science 238:1415
Lee RE, McGrath JJ, Todd Morason R, Taddeo RM (1993) Survival of intracellular freezing, lipid coalescence and osmotic fragility in fat body cells of the freeze-tolerant gall fly Eurosta solidaginis. J Insect Physiol 39:445–450
Lee MR, Lee RE Jr, Strong-Gunderson JM, Minges SR (1995) Isolation of ice-nucleating active bacteria from the freeze-tolerant frog, Rana sylvatica. Cryobiology 32:358–365
Lee JK, Park KS, Park S, Park H, Song YH, Kang S-H, Kim HJ (2010) An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 60:222–228
Lee RE Jr (2010) A primer on insect cold-tolerance. Cambridge University Press, Cambridge
Lee RE Jr, Costanzo JP (1998) Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annu Rev Physiol 60:55–72
Lee RE Jr, Lewis EA (1985) Effect of temperature and duration of exposure on tissue ice formation in the gall fly Eurosta solidaginis diptera tephritidae. Cryo Letters 6:25–34
Lee RE Jr, Elnitsky MA, Rinehart JP, Hayward SAL, Sandro LH, Denlinger DL (2006a) Rapid cold-hardening increases the freezing tolerance of the Antarctic midge Belgica antarctica. J Exp Biol 209:399
Lee RE Jr, Damodaran K, Yi SX, Lorigan GA (2006b) Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52:459–463
Li N, Andorfer CA, Duman JG (1998) Enhancement of insect antifreeze protein activity by solutes of low molecular mass. J Exp Biol 201:2243–2251
Loomis SH (1985) Seasonal changes in the freezing tolerance of the intertidal pulmonate gastropod Melampus bidentatus say. Can J Zool 63:2021–2025
Low W-K, Lin Q, Ewart KV, Fletcher GL, Hew CL (2002) The skin-type antifreeze polypeptides: a new class of type I AFPs. In: Fish antifreeze proteins, vol 1. World Scientific, River Edge, NJ, pp 161–186
Luzardo MC, Amalfa F, Nunez AM, Diaz S, Biondi De Lopez AC, Disalvo EA (2000) Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys J 78:2452–2458
Lytvyak E, Olstad DL, Schopflocher DP, Plotnikoff RC, Storey KE, Nykiforuk CI, Raine KD (2016) Impact of a 3-year multi-centre community-based intervention on risk factors for chronic disease and obesity among free-living adults: the healthy Alberta communities study. BMC Public Health 16:344
Mackenzie AP, Derbyshire W, Reid DS, Richards Rex E, Franks F (1977) Non-equilibrium freezing behaviour of aqueous systems. Philos Trans R Soc Lond B Biol Sci 278:167–189
MacMillan HA, Findsen A, Pedersen TH, Overgaard J (2014) Cold-induced depolarization of insect muscle: differing roles of extracellular K+ during acute and chronic chilling. J Exp Biol 217:2930–2938
Marshall KE, Sinclair BJ (2011) The sub-lethal effects of repeated freezing in the woolly bear caterpillar Pyrrharctia isabella. J Exp Biol 214:1205–1212
Martino M, Otero L, Sanz P, Zaritzky N (1998) Size and location of ice crystals in pork frozen by high-pressure-assisted freezing as compared to classical methods. Meat Sci 50(3):303–313
Mazur P (1977) The role of intracellular freezing in the death of cells cooled at supraoptimal rates. Cryobiology 14:251–272
Mazur P, Leibo SP, Chu EH (1972) A two-factor hypothesis of freezing injury. Evidence from Chinese hamster tissue-culture cells. Exp Cell Res 71:345–355
Meier P, Zettel J (1997) Cold hardiness in Entomobrya nivalis (Collembola, Entomobryidae): annual cycle of polyols and antifreeze proteins, and antifreeze triggering by temperature and photoperiod. J Comp Physiol B 167:297–304
Mellanby K, Gardiner JS (1939) Low temperature and insect activity. Proc R Soc L Ser B 127:473–487
Meryman HT (1970) The exceeding of a minimum tolerable cell volume in hypertonic suspension as a cause of freezing injury. In: Ciba foundation symposium - the frozen cell. Ciba, Churchill, pp 51–67
Mesa ML, Vacchi M (2001) Age and growth of high Antarctic notothenioid fish. Antarct Sci 13:227–235
Michaud MR, Benoit JB, Lopez-Martinez G, Elnitsky MA, Lee RE, Denlinger DL (2008) Metabolomics reveals unique and shared metabolic changes in response to heat shock, freezing and desiccation in the Antarctic midge, Belgica antarctica. J Insect Physiol 54:645–655
Miller LK, Smith JS (1975) Production of threitol and sorbitol by an adult insect: association with freezing tolerance. Nature 258:519–520
Miller LK, Werner R (1987) Extreme supercooling as an overwintering strategy in three species of willow gall insects from interior Alaska USA. Oikos 49:253–260
Morris GJ, Clarke A (1987) Cells at low temperatures. In: Grout BWW, Morris GJ (eds) The effects of low temperatures on biological systems. Edward Arnold, London, pp 72–119
Morrissey RE, Baust JG (1976) The ontogeny of cold tolerance in the gall fly, Eurosta solidagensis. J Insect Physiol 22:431–437
Mugnano J, Lee R, Taylor R (1996) Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze-tolerant larvae of the gall fly Eurosta solidaginis (Diptera, Tephritidae). J Exp Biol 199:465–471
Neven LG, Duman JG, Beals JM, Castellino FJ (1986) Overwintering adaptations of the stag beetle, Ceruchus piceus: removal of ice nucleators in the winter to promote supercooling. J Comp Physiol B 156:707–716
Newsted JW, Polvi S, Papish B, Kendall E, Saleem M, Koch M, Hussain A, Cutler AJ, Georges F (1994) A low molecular weight peptide from snow mold with epitopic homology to the winter flounder antifreeze protein. Biochem Cell Biol 72:152–156
Nickell PK, Sass S, Verleye D, Blumenthal EM, Duman JG (2013) Antifreeze proteins in the primary urine of larvae of the beetle Dendroides canadensis. J Exp Biol 216:1695–1703
O’Grady SM, DeVries AL (1982) Osmotic and ionic regulation in polar fishes. J Exp Mar Biol Ecol 57:219–228
Olsen TM, Duman JG (1997) Maintenance of the supercooled state in the gut fluid of overwintering pyrochroid beetle larvae, Dendroides canadensis : role of ice nucleators and antifreeze proteins. J Comp Physiol B 167:114–122
Olsen T, Sass S, Li N, Duman J (1998) Factors contributing to seasonal increases in inoculative freezing resistance in overwintering fire-colored beetle larvae Dendroides canadensis. J Exp Biol 201(Pt 10):1585–1594
Overgaard J, MacMillan HA (2017) The integrative physiology of insect chill tolerance. Annu Rev Physiol 79:187–208
Pessin JE, Bell GI (1992) Mammalian facilitative glucose transporter family: structure and molecular regulation. Annu Rev Physiol 54:911–930
Philip BN, Kiss AJ, Lee RE Jr (2011) The protective role of aquaporins in the freeze-tolerant insect Eurosta solidaginis: functional characterization and tissue abundance of EsAQP1. J Exp Biol 214:848–857
Præbel K, Hunt B, Hunt LH, DeVries AL (2009) The presence and quantification of splenic ice in the McMurdo Sound Notothenioid fish, Pagothenia borchgrevinki (Boulenger, 1902). Comp Biochem Physiol A Mol Integr Physiol 154:564–569
Ramlov H (1999) Microclimate and variations in haemolymph composition in the freezing-tolerant New Zealand alpine weta Hemideina maori Hutton (Orthoptera : Stenopelmatidae). J Comp Physiol B 169:224–235
Ramlov H (2000) Aspects of natural cold tolerance in ectothermic animals. Hum Reprod 15(Suppl 5):26–46
Ramlov H, Westh P (1993) Ice formation in the freeze-tolerant alpine weta Hemideina maori Hutton (Orthoptera, Stenopelmatidae). Cryo-Letters 14:169–176
Ramlov H, Bedford J, Leader J (1992) Freezing tolerance of the New-Zealand Alpine weta, Hemideina maori Hutton [Orthoptera, Stenopelmatidae]. J Therm Biol 17:51–54
Ramlov H, Wharton DA, Wilson PW (1996) Recrystallization in a freezing tolerant antarctic nematode, Panagrolaimus davidi, and an alpine weta, Hemideina maori (Orthoptera: Stenopelmatidae). Cryobiology 33:607–613
Raymond JA, Fritsen CH (2001) Semipurification and ice recrystallization inhibition activity of ice-active substances associated with Antarctic photosynthetic organisms. Cryobiology 43:63–70
Raymond MR, Wharton DA (2016) The ability to survive intracellular freezing in nematodes is related to the pattern and distribution of ice formed. J Exp Biol 219:2060–2065
Raymond JA, Janech MG, Fritsen CH (2009) Novel ice-binding proteins from a psychrophilic Antarctic alga (Chlamydomonadaceae, chlorophyceae)1. J Phycol 45:130–136
Rojek A, Praetorius J, Frokiaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327
Rudolph AS, Crowe JH (1985) Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline. Cryobiology 22:367–377
Rudolph AS, Crowe JH, Crowe LM (1986) Effects of three stabilizing agents--proline, betaine, and trehalose--on membrane phospholipids. Arch Biochem Biophys 245:134–143
Salt RW (1961) Principles of insect cold-hardiness. Annu Rev Entomol 6:55–74
Scholander PF, Flagg W, Hock RJ, Irving L (1953) Studies on the physiology of frozen plants and animals in the Arctic. J Cell Physiol Suppl 42:1–56
Semper K (1883) Natural conditions of existence as they affect animal life. Kegan Paul, Trench & CO., London
Sformo T, Walters K, Jeannet K, Wowk B, Fahy GM, Barnes BM, Duman JG (2010) Deep supercooling, vitrification and limited survival to −100{degrees}C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. J Exp Biol 213:502–509
Shimada K, Riihimaa A (1988) Cold acclimation, inoculative freezing and slow cooling: essential factors contributing to the freezing-tolerance in diapausing larvae of Chymomyza costata. Drosophilidae, Diptera
Sidebottom CM, Smallwood MF, Byass LJ (1999) Frozen product, vol. WO99/37673
Sinclair BJ, Klok CJ, Scott MB, Terblanche JS, Chown SL (2003) Diurnal variation in supercooling points of three species of Collembola from Cape Hallett, Antarctica. J Insect Physiol 49:1049–1061
Sinclair BJ, Klok CJ, Chown SL (2004) Metabolism of the sub-Antarctic caterpillar Pringleophaga marioni during cooling, freezing and thawing. J Exp Biol 207:1287–1294
Sinclair BJ, Gibbs AG, Lee WK, Rajamohan A, Roberts SP, Socha JJ (2009) Synchrotron x-ray visualisation of ice formation in insects during lethal and non-lethal freezing. PLoS One 4(12):e8259
Sømme L (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A Mol Integr Physiol 73:519–543
Sømme L, Zachariassen KE (1981) Adaptations to low temperature in high altitude insects from Mount Kenya. Ecol Entomol 6:199–204
Storey KB (2004) Strategies for exploration of freeze responsive gene expression: advances in vertebrate freeze tolerance. Cryobiology 48:134–145
Storey JM, Storey KB (1985) Freezing and cellular metabolism in the gall fly larva, Eurosta solidaginis. J Comp Physiol B 155:333–337
Storey KB, Storey JM (1988) Freeze tolerance in animals. Physiol Rev 68:27–84
Storey KB, Storey JM (1992) Natural freeze tolerance in ectothermic vertebrates. Annu Rev Physiol 54:619–637
Storey KB, Storey JM (1993) Cellular adaptations for freezing survival of amphibians and reptiles, vol 2. JAI Press, London, pp 101–129
Storey KB, Storey JM (1996) Natural freezing survival in animals. Annu Rev Ecol Syst 27:365–386
Storey KB, Storey JM (2013) Molecular biology of freezing tolerance. Compr Physiol 3:1283–1308
Tantos A, Friedrich P, Tompa P (2009) Cold stability of intrinsically disordered proteins. FEBS Lett 583:465–469
Taylor MJ (1987) Physico-chemical principles in low temperature biology. In: Grout BWW, Morris GJ (eds) The effects of low temperatures on biological systems. Edmond Arnold, London, pp 3–71
Teets NM, Denlinger DL (2013) Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiol Entomol 38:105–116
Teets NM, Kawarasaki Y, Lee RE Jr, Denlinger DL (2011) Survival and energetic costs of repeated cold exposure in the Antarctic midge, Belgica antarctica: a comparison between frozen and supercooled larvae. J Exp Biol 214:806–814
Teets NM, Yi SX, Lee RE Jr, Denlinger DL (2013) Calcium signaling mediates cold sensing in insect tissues. Proc Natl Acad Sci U S A 110:9154–9159
Toxopeus J, Sinclair BJ (2018) Mechanisms underlying insect freeze tolerance. Biol Rev Camb Philos Soc 93:1891–1914
Tsumuki H (2000) Review of low temperature tolerance and ice nuclei in insects, with special emphasis on larvae of the rice stem borer, Chilo suppressalis Walker. Jpn J Appl Entomol Zool 44(3):149–154
Tsumuki H, Konno H (1991) Tissue distribution of the ice-nucleating agents in larvae of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae). Cryobiology 28(4):376–381
Turner JD, Schrag JD, Devries AL (1985) Ocular freezing avoidance in antarctic fish. J Exp Biol 118:121
Tursman D, Duman JG (1995) Cryoprotective effects of thermal hysteresis protein on survivorship of frozen gut cells from the freeze-tolerant centipede Lithobius forficatus. J Exp Zool 272(4):249–257
Vali G (1995) Principles of ice nucleation. APS Press, St. Paul, pp 1–28
van der Laak S (1982) Physiological adaptations to low temperature in freezing-tolerant Phyllodecta laticollis beetles. Comp Biochem Physiol A Physiol 73:613–620
Voituron Y, Paaschburg L, Holmstrup M, Barre H, Ramlov H (2009) Survival and metabolism of Rana arvalis during freezing. J Comp Physiol B 179:223–230
Waagner D, Bouvrais H, Ipsen JH, Holmstrup M (2013) Linking membrane physical properties and low temperature tolerance in arthropods. Cryobiology 67:383–385
Webb MS, Uemura M, Steponkus PL (1994) A comparison of freezing injury in oat and rye: two cereals at the extremes of freezing tolerance. Plant Physiol 104:467
Wharton DA, Ferns DJ (1995) Survival of intracellular freezing by the Antarctic nematode Panagrolaimus davidi. J Exp Biol 198:1381–1387
Wharton DA, Barrett J, Goodall G, Marshall CJ, Ramlov H (2005) Ice-active proteins from the Antarctic nematode Panagrolaimus davidi. Cryobiology 51:198–207
Wharton DA, Pow B, Kristensen M, Ramlov H, Marshall CJ (2009) ICE-active proteins and cryoprotectants from the New Zealand alpine cockroach, Celatoblatta quinquemaculata. J Insect Physiol 55:27–31
Wilkens C, Ramlov H (2008) Seasonal variations in antifreeze protein activity and haemolymph osmolality in larvae of the beetle Rhagium mordax (Coleoptera : Cerambycidae). CryoLetters 29:293–300
Wilson PW, Leader JP (1995) Stabilization of supercooled fluids by thermal hysteresis proteins. Biophys J 68:2098–2107
Wilson P, Ramlov H (1995) Hemolymph ice nucleating proteins from the New-Zealand alpine Weta Hemideina maori (Orthoptera, Stenopelmatidae). Comp Biochem Physiol B 112:535–542
Wilson PW, Heneghan AF, Haymet AD (2003) Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46:88–98
Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524
Worland MR, Block WI, Grubor-Lajsic G (2000) Survival of Heleomyza borealis (Diptera, Heleomyzidae) larvae down to − 60°C. Physiol Entomol 25:1–5
Worland MR, Wharton DA, Byars SG (2004) Intracellular freezing and survival in the freeze tolerant alpine cockroach Celatoblatta quinquemaculata. J Insect Physiol 50:225–232
Yamashita Y, Nakamura N, Omiya K, Nishikawa J, Kawahara H, Obata H (2002) Identification of an antifreeze lipoprotein from Moraxella sp. of Antarctic origin. Biosci Biotechnol Biochem 66:239–247
Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830
Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222
Yi SX, Lee RE Jr (2003) Detecting freeze injury and seasonal cold-hardening of cells and tissues in the gall fly larvae, Eurosta solidaginis (Diptera: Tephritidae) using fluorescent vital dyes. J Insect Physiol 49:999–1004
Zachariassen KE (1973) Seasonal variation in hemolymph osmolality and osmotic contribution of glycerol in adult Rhagium inquisitor L. (Col., Cerambycidae). Cryo Letters 29(4):293–300
Zachariassen KE (1979) The mechanism of the cryoprotective effect of glycerol in beetles tolerant to freezing. J Insect Physiol 25:29–32
Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799–832
Zachariassen KE, Hammel HT (1976) Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262:285–287
Zachariassen KE, Husby JA (1982) Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 298:865–867
Zachariassen KE, Kristiansen E (2000) Ice nucleation and antinucleation in nature. Cryobiology 41:257–279
Zachariassen KE, Kristiansen E, Pedersen SA, Hammel HT (2004) Ice nucleation in solutions and freeze-avoiding insects-homogeneous or heterogeneous? Cryobiology 48:309–321
Zachariassen KE, Li NG, Laugsand AE, Kristiansen E, Pedersen SA (2008) Is the strategy for cold hardiness in insects determined by their water balance? A study on two closely related families of beetles: Cerambycidae and Chrysomelidae. J Comp Physiol B 178:977–984
Zimmerman SL, Frisbie J, Goldstein DL, West J, Rivera K, Krane CM (2007) Excretion and conservation of glycerol, and expression of aquaporins and glyceroporins, during cold acclimation in Cope’s gray tree frog Hyla chrysoscelis. Am J Physiol Regul Integr Comp Physiol 292:R544–R555
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Ramløv, H., Friis, D.S. (2020). Ice Formation in Living Organisms. In: Ramløv, H., Friis, D. (eds) Antifreeze Proteins Volume 1. Springer, Cham. https://doi.org/10.1007/978-3-030-41929-5_4
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