Skip to main content Accessibility help
×
Hostname: page-component-6b989bf9dc-g5k2d Total loading time: 0 Render date: 2024-04-14T12:21:08.372Z Has data issue: false hasContentIssue false

3 - Antifreeze and ice-nucleator proteins

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

Published online by Cambridge University Press:  04 May 2010

David L. Denlinger
Affiliation:
Ohio State University
Richard E. Lee, Jr
Affiliation:
Miami University
Get access

Summary

Introduction

Supercooling ability is a critical component among the suite of adaptations contributing to subzero temperature-tolerance of insects, whether they follow freeze-tolerance or freeze-avoidance strategies. Supercooling points (SCP, nucleation temperature, or crystallization temperature) of insects and other terrestrial arthropods range tremendously, from −2 °C to −100 °C or lower. Supercooling is affected by a number of factors, including the volume and water content of the organism, and the ability of the body surface to prevent inoculative freezing by external ice. However, the topics of this review, ice nucleators and antifreeze proteins, are often of critical importance. Antifreezes can be both small-molecular-mass solutes, such as polyhydroxyl alcohols that depress the freezing point of water on a strictly colligative basis, and high-molecular-mass molecules such as antifreeze proteins that suppress freezing by a non-colligative mechanism. Freeze-tolerant species often exhibit high SCPs (above −10 °C) and have selected for extracellular ice nucleators, while freeze-avoiding insects generally have selected against ice nucleators and for antifreezes, allowing them to supercool below ambient temperatures to which they are exposed over the winter. This review will attempt to provide a broad update on ice nucleators, antifreeze proteins and related adaptations in insects and other arthropods, primarily from the standpoint of how they function in organisms to promote winter survival.

Protein ice nucleators

Ice nucleators (INs) limit supercooling by organizing water into an ice-like structure, the embryo crystal, that promotes freezing at a temperature higher than that where ice would otherwise form (Knight, 1967).

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amornwittawat, N., Wang, S., Duman, J. G., and Wen, X. (2008) Polycarboxylates enhance beetle antifreeze protein activity. Biochimica et Biophysica Acta, Proteins and Proteomics 1784, 1942–1948.CrossRefGoogle ScholarPubMed
Amornwittawat, N., Wang, S., Banatlao, J., Chung, M., Velasco, E., Duman, J. G., and Wen, X. (2009). Effects of polyhydroxy compounds on beetle antifreeze protein activity. Biochimica et Biophysica Acta, Proteins, and Proteomics 1794, 341–346.CrossRefGoogle ScholarPubMed
Andorfer, C. A. and Duman, J. G. (2000). Isolation and characterization of cDNA clones endcoding antifreeze proteins of the pyrochroid beetle Dendroides canadensis. Journal of Insect Physiology 46, 365–372.CrossRefGoogle Scholar
Bale, J. S., Hansen, T. N., and Baust, J. G. (1989). Nucleators and sites of nucleation in the freeze tolerant larvae of the gallfly Eurosta solidaginis (Fitch). Journal of Insect Physiology 35, 291–298.CrossRefGoogle Scholar
Bale, J. S., Worland, M. R., and Block, W. (2000). Thermal tolerance and acclimation response of the subAntarctic beetle Hydromedion sparsutum. Polar Biology 23, 77–84.CrossRefGoogle Scholar
Bennett, V. A., Sformo, T., Walters, K., Toien, O., Jeannet, K., Hochstrasser, R., Pan, Q., Serianni, A. S., Barnes, B. M., and Duman, J. G. (2005). Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricus): Roles of antifreeze proteins, polyols, dehydration, and diapause. Journal of Experimental Biology 208: 4467–4477.CrossRefGoogle Scholar
Bigg, E. K. (1953). The supercooling of water. The Physical Society 66, 688–691.CrossRefGoogle Scholar
Block, W. and Duman, J. G. (1989). The presence of thermal hysteresis producing antifreeze proteins in the Antarctic mite, Alaskozetes antarcticus. Journal of Experimental Zoology 250, 229–231.CrossRefGoogle Scholar
Brown, C. L., Bale, J. S., and Walters, K. F. A. (2004). Freezing induces a loss of freeze tolerance in an overwintering insect. Proceedings of the Royal Society, Series B 271, 1507–1511.CrossRefGoogle Scholar
Cannon, R. J. C. and Block, W. (1988). Cold tolerance of microarthropods. Biological Reviews of the Cambridge Philosophical Society 63, 23–77.CrossRefGoogle Scholar
DeVries, A. L. (1971). Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172, 1152–1155.CrossRefGoogle ScholarPubMed
DeVries, A. L. (1986). Antifreeze glycopeptides and peptides: Interactions with ice and water. Methods in Enzymology 127, 293–303.CrossRefGoogle Scholar
DeVries, A. L. and Cheng, C.-H. C. (1992). The role of antifreeze glycopeptides and peptides in the survival of cold-water fishes. In Water and Life, ed. Somero, G. N., Osmond, C. B. and Bolis, C. L.. Berlin, Heidelberg: Springer-Verlag, pp. 301–315.CrossRefGoogle Scholar
DeVries, A. L., Komatsu, S. K., and Feeney, R. E. (1970). Chemical and physical properties of freezing point depressing glycoproteins from Antarctic fishes. Journal of Biological Chemistry 245, 2901–2913.Google ScholarPubMed
DeVries, A. L. and Wohlschlag, (1969) Freezing resistance in some Antarctic fishes. Science 163, 1073–1075.CrossRefGoogle ScholarPubMed
Doucet, D., Tyshenko, M. G., Davies, P. L., and Walker, V. K. (2001). A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. European Journal of Biochemistry 269, 38–46.CrossRefGoogle Scholar
Duman, J, G. (1977a). The role of macromolecular antifreeze in the darkling beetle, Meracantha contracta. Journal of Comparative Physiology B 115, 279–286.CrossRefGoogle Scholar
Duman, J. G. (1977b). Variations in macromolecular antifreeze levels in larvae of the darkling beetle, Meracantha contracta. Journal of Experimental Zoology, 85–93.CrossRefGoogle ScholarPubMed
Duman, J. G. (1979a). Thermal hysteresis factors in overwintering insects. Journal of Insect Physiology 25, 805–810.CrossRefGoogle Scholar
Duman, J. G. (1979b). Subzero temperature tolerance in spiders: The role of thermal hysteresis factors. Journal of Comparative Physiology B 131, 347–352.CrossRefGoogle Scholar
Duman, J. G. (1984). Thermal hysteresis antifreeze proteins in the midgut fluid of overwintering larvae of the beetle Dendroides canadensis. Journal of Experimental Zoology 230, 355–361.CrossRefGoogle Scholar
Duman, J. G. (2001). Antifreeze and ice nucleator proteins in terrestrial arthropods. Annual Review of Physiology 63, 327–355.CrossRefGoogle ScholarPubMed
Duman, J. G. (2002). The inhibition of ice nucleators by insect antifreeze proteins is enhanced by glycerol and citrate. Journal of Comparative Physiology B 172, 163–168.Google ScholarPubMed
Duman, J. G., Bennett, V., Sformo, T., Hochstrasser, R., and Barnes, B. M. (2004a). Antifreeze proteins in Alaskan insects and spiders. Journal of Insect Physiology 50, 259–266.CrossRefGoogle ScholarPubMed
Duman, J. G., Bennett, V. A., Li, N., Wang, L., Huang, L., Sformo, T., and Barnes, B. M. (2004b). Antifreeze proteins in terrestrial arthropods. In Life in the Cold, ed. Barnes, B. M. and Carey, H. V.. University of Alaska Press, pp. 527–542.Google Scholar
Duman, J. G. and DeVries, A. L. (1974). Freezing resistance in winter flounder, Pseudopleuronectes americanus. Nature 247, 237–238.CrossRefGoogle Scholar
Duman, J. G. and DeVries, A. L. (1975). The role of macromolecular antifreeze in cold water fishes. Comparative Biochemistry and Physiology 52A, 193–199.CrossRefGoogle Scholar
Duman, J. G. and DeVries, A. L. (1976) The isolation, characterization and physical properties of protein antifreeze from winter flounder, Pseudopleuronectes americanus. Comparative Biochemistry and Physiology 54B, 375–380.Google Scholar
Duman, J. G., Neven, L. G., Beals, J. M., Olson, K. R., and Castellino, F. J. (1985). Freeze tolerance adaptations, including haemolymph protein and lipoprotein ice nucleators, in larvae of the cranefly Tipula trivittata. Journal of Insect Physiology 31, 1–9.CrossRefGoogle Scholar
Duman, J. G., Parmalee, D., Goetz, F. W., Li, N., Wu, D. W., and Benjamin, T. (1998). Molecular characterization and sequencing of antifreeze proteins from larvae of the beetle Dendroides canadensis. Journal of Comparative Physiology B 168, 225–232.CrossRefGoogle ScholarPubMed
Duman, J. G. and Patterson, J. L. (1978). The role of ice nucleators in the frost tolerance of queens of the bald-faced hornet Vespula maculata. Comparative Physiology and Biochemistry 59A, 69–72.CrossRefGoogle Scholar
Duman, J. G. and Serianni, A. S. (2002). The role of endogenous antifreeze protein enhancers in the hemolymph thermal hysteresis activity of the beetle Dendroides canadensis. Journal of Insect Physiology 48, 103–111.CrossRefGoogle ScholarPubMed
Duman, J. G., Wu, D. W., Yeung, K. L., and Wolf, E. E. (1992). Hemolymph proteins involved in the cold tolerance of terrestrial arthropods; Antifreeze and ice nucleator proteins. In Water and Life, ed. Somero, G. N. and Osmond, C. B.. Berlin: Springer-Verlag, pp. 282–300.CrossRefGoogle Scholar
Duman, J. G., Wu, D. W., Olsen, T. M., Urrutia, M., and Tursman, D. (1993). Thermal hysteresis proteins. Advances in Low Temperature Biology 2, 131–182.Google Scholar
Duman, J. G., Xu, L. X., Neven, L. G., Tursman, D., and Wu, D. W. (1991). Hemolymph proteins involved in insect subzero temperature tolerance: Ice nucleators and antifreeze proteins. In Insects at Low Temperatures, ed. Lee, R. E. and Denlinger, D. L.. New York and London: Chapman and Hall, pp. 94–127.CrossRefGoogle Scholar
Duman, J. G., Verleye, D., and Li, N. (2002). Site specific forms of antifreeze proteins in the beetle Dendroides canadensis. Journal of Comparative Physiology B 172, 547–552.Google ScholarPubMed
Fields, P. G. and McNeil, J. N. (1986). Possible dual cold-hardiness strategies in Cisseps fulvicolis (Lepidoptera: Arctiidae). Canadian Journal of Entomology 118, 1309–1311.CrossRefGoogle Scholar
Gauthier, S. Y., Kay, C. M., Sykes, B. D., Walker, V. K., and Davies, P. L. (1998). Disulfide bond mapping and structural characterization of spruce budworm antifreeze protein. European Journal of Biochemistry 258, 445–453.CrossRefGoogle ScholarPubMed
Govindarajan, A. G. and Lindow, S. E. (1988). Phospholipid requirement for expression of ice nuclei in Pseudomonas syringae and in vitro. Journal of Biological Chemistry 263, 9333–9338.Google ScholarPubMed
Graether, S. P., Kuiper, M. J., Gagne, S. M., Walker, V. K., Jia, Z., Sykes, B. D., and Davies, P. L. (2000). Beta-helix structure of a hyperactive antifreeze protein from an insect. Nature 406, 325–328.CrossRefGoogle ScholarPubMed
Graether, S. P. and Sykes, B. D. (2004). Cold survival of freeze intolerant insects: The structure and function of beta-helical antifreeze proteins. European Journal of Biochemistry 271, 3285–3296.CrossRefGoogle ScholarPubMed
Graether, S. P., Ye, Q. L., Davies, P. L., and Sykes, D. B. (1999). Crystallization and preliminary x-ray crystallographic analysis of spruce budworm antifreeze protein. Journal of Structural Biology 126, 72–75.CrossRefGoogle ScholarPubMed
Graham, L. A. and Davies, P. L. (2005). Glycine-rich antifreeze proteins from snow fleas. Science 310, 461.CrossRefGoogle ScholarPubMed
Graham, L. A., Liou, Y.-C., Walker, V. K., and Davies, P. L. (1997). Hyperactive antifreeze proteins from beetles. Nature 188, 727–728.CrossRefGoogle Scholar
Graham, L. A., Walker, V. K., and Davies, P. L. (2000). Developmental and environmental regulation of antifreeze proteins in the mealworm beetle Tenebrio molitor. European Journal of Biochemistry 267, 6452–6458.CrossRefGoogle ScholarPubMed
Green, R. L. and Warren, G. J. (1985). Physical and functional repetition in a bacterial ice nucleation gene. Nature 317, 645–648.CrossRefGoogle Scholar
Griffith, M. and Yaish, M. W. (2004). Antifreeze proteins in overwintering plants: A tale of two activities. Trends in Plant Sciences 9, 399–405.CrossRefGoogle ScholarPubMed
Grimstone, A. V., Mullinger, A. M., and Ramsay, J. A. (1968). Further studies on the rectal complex of the mealworm, Tenebrio molitor. Philosophical Transactions of the Royal Society of London, Series B 248, 344–282.Google Scholar
Hansen, T. N. and Baust, J. G. (1988). Differential scanning calorimetric analysis of antifreeze protein activity in the common mealworm, Tenebrio molitor. Biochimica and Biophysica Acta-Protein Structure and Molecular Enzymology 957, 217–221.CrossRefGoogle ScholarPubMed
Hansen, T. N. and Baust, J. G. (1989). Differential scanning calorimetric analysis of Tenebrio molitor antifreeze protein activity. Cryobiology 26, 383–388.CrossRefGoogle Scholar
Horwath, K. L. and Duman, J. G. (1982). Involvement of the circadian system in photoperiodic regulation of insect antifreeze proteins. Journal of Experimental Zoology 219, 267–270.CrossRefGoogle Scholar
Horwath, K. L. and Duman, J. G. (1983a). Photoperiodic and thermal regulation of antifreeze protein levels in the beetle Dendroides canadensis. Journal of Insect Physiology 29, 907–917.CrossRefGoogle Scholar
Horwath, K. L. and Duman, J. G. (1983b). Induction of antifreeze production by juvenile hormone in larvae of the beetle Dendroides canadensis. Journal of Comparative Physiology B 151, 233–240.CrossRefGoogle Scholar
Horwath, K. L. and Duman, J. G. (1984a). Yearly variations in the overwintering mechanism of the cold hardy beetle, Dendroides canadensis. Physiological Zoology 57, 40–45.CrossRefGoogle Scholar
Horwath, K. L. and Duman, J. G. (1984b). Further studies on the involvement of the circadian system in photoperiodic control of antifreeze protein production in the beetle Dendroides canadensis. Journal of Insect Physiology 30, 947–955.CrossRefGoogle Scholar
Horwath, K. L. and Duman, J. G. (1986). Thermoperiodic involvement in antifreeze protein production in the cold hardy beetle Dendroides canadensis: Implications for photoperiodic timer measurement. Journal of Insect Physiology 32, 799–806.CrossRefGoogle Scholar
Huang, T. and Duman, J. G. (2002). Cloning and characterization of a thermal hysteresis/antifreeze protein with DNA-binding activity from winter bittersweet nightshade, Solanum dulcamara. Plant Molecular Biology 48, 339–350.CrossRefGoogle ScholarPubMed
Huang, T., Nicodemus, J., Zarka, D. G., Thomashow, M. F., and Duman, J. G. (2002). Expression of an insect (Dendroides canadensis) antifreeze protein in Arabidopsis thaliana results in a decrease in plant freezing temperature. Plant Molecular Biology 50, 333–344.CrossRefGoogle Scholar
Husby, J. A. and Zachariassen, K. E. (1980). Antifreeze agents in the body fluid of winter active insects and spiders. Experientia 36, 963–964.CrossRefGoogle Scholar
Jia, X. and Davies, P. L. (2002). Antifreeze proteins: An unusual receptor-ligand interaction. Trends in Biochemical Sciences 27, 101–106.CrossRefGoogle ScholarPubMed
Knight, C. A. (1967). The Freezing of Supercooled Liquids. New York: VanNostrand.Google Scholar
Knight, C. A., Cheng, C. C., and DeVries, A. L. (1991). Adsorption of alpha-helical antifreeze peptides on specific ice crystal surface planes. Biophysical Journal 59, 409–418.CrossRefGoogle ScholarPubMed
Knight, C. A., DeVries, A. L., and Oolman, L. D. (1984). Fish antifreeze protein and the freezing and recrystallization of ice. Nature 308, 295–296.CrossRefGoogle ScholarPubMed
Knight, C. A. and Duman, J. G. (1986). Inhibition of recrystallization of ice by insect thermal hysteresis proteins: A possible cryoprotective role. Cryobiology 23, 256–262.CrossRefGoogle Scholar
Knight, C. A., Wen, D., and Laursen, R. A. (1995). Non-equilibrium antifreeze proteins and the recrystallization of ice. Cryobiology 32, 23–34.CrossRefGoogle Scholar
Kristainsen, E., Pedersen, S. L., Ramlov, H., and Zachariassen, K. E. (1999). Antifreeze activity in the cerambycid beetle Rhagium inquisitor. Journal of Comparative Physiology B 160, 55–60.CrossRefGoogle Scholar
Kristiansen, E., Ramlov, H., Hagen, L., Pedersen, S. L., Andersen, R. A., and Zachariassen, K. E. (2005). Isolation and characterization of hemolymph antifreeze proteins from larvae of the longhorn beetle Rhagium inquisitor (L). Comparative Biochemistry and Physiology B 142, 90–97.CrossRefGoogle Scholar
Kristiansen, E. and Zachariassen, K. E. (2005). The mechanism by which fish antifreeze proteins cause thermal hysteresis. Cryobiology 51, 262–280.CrossRefGoogle ScholarPubMed
Kukal, O., Serianni, A. S., and Duman, J. G. (1988). Glycerol production in a freeze tolerant arctic insect, Gynaephora groenlandica: An in vivo13C NMR study. Journal of Comparative Physiology B 158, 175–183.CrossRefGoogle Scholar
Lee, R. E., Costanzo, J. P., and Mugnano, J. A. (1996). Regulation of supercooling and ice nucleation in insects. European Journal of Entomology 93, 405–418.Google Scholar
Leinala, E. K., Davies, P. L., Doucet, D., Tyshenko, M. G., Walker, V. K., and Jia, Z. (2002). A beta-helical antifreeze protein isoform with increased activity: Structural and functional insights. Journal of Biological Chemistry 277, 33349–33352.CrossRefGoogle ScholarPubMed
Li, N., Andorfer, C. A., and Duman, J. G. (1998b). Enhancement of insect antifreeze protein activity by low molecular mass solutes. Journal of Experimental Biology 201, 2243–2251.Google ScholarPubMed
Li, N., Chibber, B. A. K., Castellino, F. J., and Duman, J. G. (1998a). Mapping of disulfide bridges in antifreeze proteins from overwintering larvae of the beetle Dendroides canadensis. Biochemistry 37, 6343–6350.CrossRefGoogle ScholarPubMed
Li, Y., Gong, H., and Park, H. Y. (2000). Purification and partial characterization of thermal hysteresis proteins from overwintering larvae the pine needle gall midge, Thecodiplosis japonensis (Diptera: Cecidomiidae) CryoLetters 21, 117–124.Google ScholarPubMed
Lin, F.- H., Graham, L. A., Campbell, R. L., and Davies, P. L. (2007). Structural modeling of snow flea antifreeze protein. Biophysical Journal 92, 1717–1723.CrossRefGoogle ScholarPubMed
Lin, Y., Duman, J. G., and DeVries, A. L. (1972). Studies on the structure and activity of low molecular weight glycoproteins from an Antarctic fish. Biochemical Biophysical Research Communications 46,87–92.CrossRefGoogle ScholarPubMed
Lindow, S. E. (1983). The role of bacterial ice nucleation in frost injury to plants. Annual Review of Phytopathology 21, 363–384.CrossRefGoogle Scholar
Lindow, S. E. (1995). Control of epiphytic ice-nucleation-active bacteria for management of plant frost injury. In Biological Ice Nucleation and Its Applications, ed. Lee, R. E., Warren, L. G. J., and Gusta, L. V.. Saint Paul: APS Press, pp. 239–256.Google Scholar
Liou, Y.-C., Thibault, P., Walker, V. K., Davies, P. L., and Graham, L. A. (1999). A complex family of highly heterogeneous and internally repetitive hyperactive antifreeze proteins from the beetle Tenebrio molitor. Biochemistry 38, 11415–11424.CrossRefGoogle ScholarPubMed
Liu, X. Y. and Du, N. (2004). Zero-sized effect of nano-particles and inverse homogeneous nucleation. The Journal of Biological Chemistry 279, 6124–6131.CrossRefGoogle ScholarPubMed
Lundheim, R. (1996). Adaptive and Incidental Ice Nucleators. Doctorate Thesis, Norwegian University of Science and Technology, Trondheim.Google Scholar
Lu, M., Wang, B., Li, Z., Fei, Y., Wei, L., and Gao, S. (2002). Differential scanning calorimetric and circular dicroistic studies on plant antifreeze proteins. Journal of Thermal Analysis and Calorimetry 67, 689–698.CrossRefGoogle Scholar
Mazur, P. (1984). Freezing of living cells: mechanisms and implications. American Journal of Physiology 247, C125–C142.CrossRefGoogle ScholarPubMed
Meier, P. and Zettel, J. (1999). Cold hardiness in Entomobrya nivalis (Collembola, Entomobryidae): Annual cycle of polyols and antifreeze proteins, and antifreeze triggering by temperature and photoperiod. Journal of Comparative Physiology B 167, 297–304.CrossRefGoogle Scholar
Meyer, K., Keil, M., and Naldrett, M. J. (1999). A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Letters 447, 171–178.CrossRefGoogle ScholarPubMed
Miller, L. K. (1969). Freezing tolerance of an adult insect. Science 166, 105–106.CrossRefGoogle ScholarPubMed
Miller, L. K. (1982). Cold hardiness strategies of some adult and immature insects overwintering in interior Alaska. Comparative Physiology and Biochemistry 73A, 595–604.CrossRefGoogle Scholar
Miller, L. K. and Werner, R. (1987). Extreme supercooling as an overwintering strategy in three species of willow gall insects from interior Alaska. Oikos 49, 253–260.CrossRefGoogle Scholar
Mueller, G. M., Wolber, P. K., and Warren, G. J. (1990). Clustering of ice nucleation protein correlates with ice nucleation activity. Cryobiology 27, 416–422.CrossRefGoogle ScholarPubMed
Mugnano, J. A., Lee, R. E., and Taylor, R. T. (1996). Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze tolerant larvae of the gall fly Eurosta solidaginis (Fitch). Journal of Experimental Biology 199, 465–471.Google Scholar
Neven, L. G., Duman, J. G., Beals, J. M., and Castellino, F. J. (1986). Overwintering adaptations of the stag beetle Ceruchus piceus: Removal of ice nucleators in winter to promote supercooling. Journal of Comparative Physiology B 156, 707–716.CrossRefGoogle Scholar
Neven, L. G., Duman, J. G., Low, M. G., Sehl, L. C., and Castellino, F. J. (1989). Purification and characterization of an insect lipoprotein ice nucleator: Evidence for the importance of phosphatidylinositol and apolipoprotein in the ice nucleator activity. Journal of Comparative Physiology B 159, 71–82.CrossRefGoogle Scholar
Nicodemus, J., O'Tousa, J. E., and Duman, J. G. (2006). Expression of a beetle, Dendroides canadensis, antifreeze protein in Drosophila melanogaster. Journal of Insect Physiology 52, 888–896.CrossRefGoogle ScholarPubMed
Olsen, T. M. and Duman, J. G. (1997a). Maintenance of the supercooled state in overwintering pyrochroid beetle larvae Dendroides canadensis: Role of hemolymph ice nucleators and antifreeze proteins. Journal of Comparative Physiology B 167, 105–113.CrossRefGoogle Scholar
Olsen, T. M. and Duman, J. G. (1997b). Maintenance of the supercooled state in the gut of overwintering pyrochroid beetle larvae, Dendroides canadensis: role of gut ice nucleators and antifreeze proteins. Journal of Comparative Physiology B, 167, 114–122.CrossRefGoogle Scholar
Olsen, T. M., Sass, S. J., Li, N., and Duman, J. G. (1998). Factors contributing to seasonal increases in inoculative freezing resistance in overwintering fire-colored beetle larvae Dendroides canadensis (Pyrochroidae). Journal of Experimental Biology 201, 1585–1594.Google Scholar
Patterson, J. L. and Duman, J. G. (1978). The role of thermal hysteresis producing proteins in the low temperature tolerance and water balance of the mealworm, Tenebrio molitor. Journal of Experimental Biology 74, 37–45.Google Scholar
Pertaya, N., Marshall, C. B., Celik, Y., Davies, P. L., and Braslovsky, I. (2008). Direct visualization of spruce budworm antifreeze protein interacting with ice: Basal plane affinity confers hyperactivity. Biophysical Journal 95, 333–341.CrossRefGoogle ScholarPubMed
Ramlov, H., DeVries, A. L., and Wilson, P. W. (2005). Antifreeze glycoproteins from the Antarctic fish Dissostichus mawsoni studied by differential scanning calorimetry (DSC) in combination with nanoliter osmometry. CryoLetters 26, 73–84.Google Scholar
Ramsay, R. A. (1964). The rectal complex of the mealworm, Tenebrio molitor L. Coleoptera, Tenebrionidae. Philosophical Transactions of the Royal Society of London, Series B 248, 279–214.CrossRefGoogle Scholar
Raymond, J. A. and DeVries, A. L. (1977). Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proceedings of the National Academy of Sciences, USA 74, 2589–2593.CrossRefGoogle ScholarPubMed
Raymond, J. A., Wilson, P. W., and DeVries, A. L. (1989). Inhibition of growth on nonbasal planes in ice by fish antifreeze. Proceedings of the National Academy of Sciences, USA 86, 881–885.CrossRefGoogle Scholar
Ring, R. A. and Tesar, D. (1980). Cold-hardiness of the arctic beetle Pytho americanus Kirby Coleoptera, Pythidae (Salpingidae). Journal of Insect Physiology 26, 763–777.CrossRefGoogle Scholar
Salt, R. W. (1953). The influence of food on cold-hardiness in insects. Canadian Entomologist 85, 261–269.CrossRefGoogle Scholar
Sformo, T., Kohl, F., McIntyre, P., Duman, J. G., and Barnes, B. M. (2009). Simultaneous freeze tolerance and avoidance in individual fungus gnats, Exechia nugatoria. Journal of Comparative Physiology B, 179, 897–902.CrossRefGoogle ScholarPubMed
Sicheri, F. and Yang, D. S. C. (1995). Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature 375, 427–431.CrossRefGoogle ScholarPubMed
Sinclair, B. J. and Chown, S. L. (2002). Haemolymph osmolality and thermal hysteresis activity in 17 species of arthropods from subAntarctic Marion Island. Polar Biology 25, 928–933.Google Scholar
Sinclair, B. J., Terblanche, J. S., Scott, M. B., Blatch, G. L., Klok, C. J., and Chown, S. L. (2006). Environmental physiology of three species of Collembola at Cape Hallett, North Victoria Land, Antarctica. Journal of Insect Physiology 52, 29–50.CrossRefGoogle Scholar
Sjursen, H. and Sømme, L. (2000). Seasonal changes in tolerance to cold and desiccation in Phauloppia sp. (Acari, Oribatidae) from Finse, Norway. Journal of Insect Physiology 46, 1387–1396.CrossRefGoogle Scholar
Smallwood, M., Worrall, D., Byass, L., Ashford, D., Doucet, C. J., Holt, C., Telford, J., Lilliford, P., and Bowles, D. J. (1999). Isolation and characterization of a novel antifreeze protein from carrot (Daucus carota)Biochemical Journal 340, 385–391.CrossRefGoogle Scholar
Sømme, L. (1978). Nucleating agents in the haemolymph of the third instar larvae of Eurosta solidaginis (Fitch) (Diptera: Tephritidae). Norwegian Journal of Entomology 25, 187–188.Google Scholar
Sømme, L. (1982). Supercooling and winter survival in terrestrial arthropods. Comparative Physiology and Biochemistry 73A, 519–543.CrossRefGoogle Scholar
Southworth, M. W., Wolber, P. K., and Warren, G. J. (1988). Nonlinear relationship between concentration and activity of a bacterial ice nucleation protein. Journal of Biological Chemistry 263, 15211–15216.Google ScholarPubMed
Thomas, M. C. (2002). Cucujidae (Latreille 1802). In American Beetles Volume 2, eds. Arnett, R. H., Thomas, M. C., Skelley, P. E., and Howard, J. H.. Boca Raton, London, New York, Washington, D.C.: CRC Press, pp. 329–330.Google Scholar
Tomczak, M. M. and Crowe, J. H. (2002). The interaction of antifreeze proteins with model membranes and cells. In Fish Antifreeze Proteins, ed. Ewart, K. V. and Hew, C. L., London: World Scientific, pp. 187–212.CrossRefGoogle Scholar
Tursman, D. and Duman, J. G. (1995). Cryoprotective effects of thermal hysteresis protein on survivorship of frozen gut cells from the freeze tolerant centipede Lithobius forficatus. Journal of Experimental Zoology 272, 249–257.CrossRefGoogle Scholar
Tursman, D., Duman, J. G., and Knight, C. A. (1994). Freeze tolerance adaptations in the centipede Lithobius forficatus. Journal of Experimental Zoology 268, 347–353.CrossRefGoogle Scholar
Tyshenko, M. G., Doucet, D., Davies, P. L., and Walker, V. K. (1997). The antifreeze potential of spruce budworm thermal hysteresis protein. Nature Biotechnology 15, 887–890.CrossRefGoogle ScholarPubMed
Urrutia, M. E., Duman, J. G., and Knight, C. A. (1992). Plant thermal hysteresis proteins. Biochimica et Biophysica Acta 1121, 199–206.CrossRefGoogle ScholarPubMed
Vanketesh, S. and Dayanada, C. (2008). Properties, potentials and prospects of antifreeze proteins. Critical Reviews of Biotechnology 28, 57–82.CrossRefGoogle Scholar
Walters, K. R., Serianni, A. S., Sformo, T., Barnes, B. M., and Duman, J. G. (2009). A novel thermal hysteresis-producing xylomannan antifreeze in a freeze tolerant Alaskan beetle. Proceedings of the National Academy of Sciences, USA (in press).CrossRef
Walters, K. R., Sformo, T., Barnes, B. M., and Duman, J. G. (2009). Freeze tolerance of an Arctic Alaska stonefly. Journal of Experimental Biology 212, 305–312.CrossRefGoogle ScholarPubMed
Wang, L. and Duman, J. G. (2005). Antifreeze proteins of the beetle Dendroides canadensis enhance one another's activities. Biochemistry 44, 10305–10312.CrossRefGoogle ScholarPubMed
Wang, L. and Duman, J. G. (2006). A thaumatin-like protein from larvae of the beetle Dendroides canadensis enhances the activity of antifreeze proteins. Biochemistry 45, 1278–1284.CrossRefGoogle ScholarPubMed
Wharton, D. A., Pow, B., Kristensen, M., Ramlov, H. R., and Marshall, C. J. (2009). Ice-active proteins and cryoprotectants from the New Zealand alpine cockroach Celatoblatta quinquemaculata. Journal of Insect Physiology 55, 27–31.CrossRefGoogle ScholarPubMed
Wilson, P. W. (1993). Explaining thermal hysteresis by the Kelvin effect. CryoLetters 14, 31–36.Google Scholar
Wolber, P. K. and Warren, G. J. (1989). Bacterial ice nucleating proteins. Trends in Biochemical Sciences 14, 179–182.CrossRefGoogle Scholar
Worral, D., Elias, L., Ashford, D., Smallwood, M., Sidebottom, C., Lilliford, P., Telford, J., Holt, C., and Bowles, D. (1998). A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 282, 115–117.CrossRefGoogle Scholar
Wu, D. W. and Duman, J. G. (1991). Activation of antifreeze proteins from the beetle Dendroides canadensis. Journal of Comparative Physiology B, 161, 279–283.CrossRefGoogle Scholar
Wu, D. W., Duman, J. G., and Xu, L. (1991). Enhancement of insect antifreeze protein activity by antibodies. Biochimica et Biophysica Acta 1076, 416–420.CrossRefGoogle ScholarPubMed
Xu, L. and Duman, J. G. (1991) Involvement of juvenile hormone in the induction of antifreeze protein production by fat body in larvae of the beetle Dendroides canadensis. Journal of Experimental Zoology 258, 288–293.CrossRefGoogle Scholar
Xu, L., Duman, J. G., Goodman, W. G., and Wu, D. W. (1992) A role for juvenile hormone in the induction of antifreeze protein production by the fat body in the beetle Tenebrio molitor. Comparative Biochemistry and Physiology 101B, 105–109.Google Scholar
Yeung, K. L., Wolf, E. E., and Duman, J. G. (1991). A scanning tunneling microscopy study of an insect lipoprotein ice nucleator. Journal of Vacuum Science and technologyB 9, 1197–1201.CrossRefGoogle Scholar
Zachariassen, K. E. (1982). Nucleating agents in cold-hardy insects. Comparative Physiology and Biochemistry 73A, 557–562.CrossRefGoogle Scholar
Zachariassen, K. E. (1985). Physiology of cold tolerance in insects. Physiological Reviews 65, 799–832.CrossRefGoogle ScholarPubMed
Zachariassen, K. E., DeVries, A. L., Hunt, B., and Kristiansen, E. (2002). Effect of ice fraction and dilution factor on the antifreeze activity in the hemolymph of the cerambycid beetle Rhagium inquisitor. Cryobiology 44, 132–141.CrossRefGoogle ScholarPubMed
Zachariassen, K. E. and Hammel, H. T. (1976). Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262, 285–287.CrossRefGoogle ScholarPubMed
Zachariassen, K. E. and Husby, J. A. (1982). Antifreeze effects of thermal hysteresis agents protect highly supercooled insects. Nature 298, 865–867.CrossRefGoogle Scholar
Zachariassen, K. E., Kristansen, E., Pedersen, S. A., and Hammel, H. T. (2004). Ice nucleation in solutions and freezing in insects – homogeneous or heterogeneous?Cryobiology 48, 309–321.CrossRefGoogle ScholarPubMed
Zachariassen, K. E., Li, N. G., Laugsand, A. E., Kristiansen, E., and Pedersen, S. A. (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. Journal of Comparative Physiology B 178, 977–984.CrossRefGoogle ScholarPubMed
Zettel, J. (1984). Cold hardiness strategies and thermal hysteresis in Collembola. Revue d'Ecologie de Biologie du Sol 21, 189–203.Google Scholar
Zhang, D. Q., Liu, B., Feng, D. R., He, Y. M., and Wang, J. F. (2004). Expression and purification of antifreeze activity of carrot antifreeze protein and its mutants. Protein Expression and Purification 35, 257–263.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×