Advertisement

Physicochemical Properties of Antifreeze Proteins

  • Dennis Steven Friis
  • Hans Ramløv
Chapter
  • 26 Downloads

Abstract

Proteins’ physicochemical properties is a broad term, and cover more than has been investigated for antifreeze proteins. In this chapter the investigations of antifreeze proteins (AFPs) are confined to weight, activity, solubility, hydrophobicity, and stability of the proteins. The weight and activity are presented together and compared, as much research suggests a positive correlation between these properties. This correlation applies for both fish AFPs and hyperactive arthropod AFPs, when comparing activity measurements within each AFP type. Not much research has focused on the solubility of AFPs, most likely due to their high solubility, which has not been inflicting with the main objective of the investigations. The AFPs are generally amphiphilic, having a relatively hydrophobic surface at the flat ice-binding region of the protein, while the rest of the proteins’ solvent-exposed surface is regarded as relatively hydrophilic. The hydrophobicity of the ice-binding site is regarded to be a key feature to bind to ice, explained by the anchored clathrate mechanism.

The AFPs are generally stable in a broad pH range. The temperature stability shows no particular pattern, as both very heat-labile and heat-stable AFPs are found. However, several AFPs have the ability to refold into an active/native form after having been unfolded due to heat exposure. Not surprisingly, the diverse group of AFPs has just as diverse physicochemical properties, with the ability to interact with ice as the only common denominator.

Keywords

Size Weight Hydrophobicity Solubility Stability Temperature pH Transition 

References

  1. Bar Dolev M, Braslavsky I, Davies PL (2016) Ice-binding proteins and their function. Annu Rev Biochem 85:515–542.  https://doi.org/10.1146/annurev-biochem-060815-014546CrossRefPubMedGoogle Scholar
  2. Bar M, Scherf T, Fass D (2008) Two-dimensional surface display of functional groups on a beta-helical antifreeze protein scaffold. Protein Eng Des Sel 21(2):107–114.  https://doi.org/10.1093/protein/gzm070CrossRefPubMedGoogle Scholar
  3. Basu K, Wasserman SS, Jeronimo PS, Graham LA, Davies PL (2016) Intermediate activity of midge antifreeze protein is due to a tyrosine-rich ice-binding site and atypical ice plane affinity. FEBS J 283(8):1504–1515.  https://doi.org/10.1111/febs.13687CrossRefPubMedGoogle Scholar
  4. Block W, Duman JG (1989) Presence of thermal hysteresis producing antifreeze proteins in the antarctic mite, Alaskozetes antarcticus. J Exp Zool 250(2):229–231.  https://doi.org/10.1002/jez.1402500215CrossRefGoogle Scholar
  5. Burcham TS, Osuga DT, Chino H, Feeney RE (1984) Analysis of antifreeze glycoproteins in fish serum. Anal Biochem 139(1):197–204CrossRefGoogle Scholar
  6. Chakrabartty A, Hew CL (1991) The effect of enhanced alpha-helicity on the activity of a winter flounder antifreeze polypeptide. Eur J Biochem 202(3):1057–1063CrossRefGoogle Scholar
  7. Chao H, Sönnichsen FD, DeLuca CI, Sykes BD, Davies PL (1994) Structure-function relationship in the globular type III antifreeze protein: identification of a cluster of surface residues required for binding to ice. Protein Sci 3(10):1760–1769.  https://doi.org/10.1002/pro.5560031016CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chao H, Hodges RS, Kay CM, Gauthier SY, Davies PL (1996) A natural variant of type I antifreeze protein with four ice-binding repeats is a particularly potent antifreeze. Protein Sci 5(6):1150–1156.  https://doi.org/10.1002/pro.5560050617CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cheng CH, DeVries AL (1989) Structures of antifreeze peptides from the Antarctic eel pout, Austrolycicthys brachycephalus. Biochim Biophys Acta 997(1–2):55–64CrossRefGoogle Scholar
  10. Cheng A, Merz KM (1997) Ice-binding mechanism of winter flounder antifreeze proteins. Biophys J 73(6):2851–2873.  https://doi.org/10.1016/S0006-3495(97)78315-2CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chi EY, Krishnan S, Randolph TW, Carpenter JF (2003) Physical stability of proteins in aqueous solution: mechanism and driving forces in nonnative protein aggregation. Pharm Res 20(9):1325–1336CrossRefGoogle Scholar
  12. Cornette JL, Cease KB, Margalit H, Spouge JL, Berzofsky JA, DeLisi C (1987) Hydrophobicity scales and computational techniques for detecting amphipathic structures in proteins. J Mol Biol 195(3):659–685CrossRefGoogle Scholar
  13. Davies PL, Baardsnes J, Kuiper MJ, Walker VK (2002) Structure and function of antifreeze proteins. Philos Trans R Soc Lond Ser B Biol Sci 357(1423):927–935.  https://doi.org/10.1098/rstb.2002.1081CrossRefGoogle Scholar
  14. DeLuca CI, Comley R, Davies PL (1998) Antifreeze proteins bind independently to ice. Biophys J 74(3):1502–1508.  https://doi.org/10.1016/S0006-3495(98)77862-2CrossRefPubMedPubMedCentralGoogle Scholar
  15. Deng G, Laursen RA (1998) Isolation and characterization of an antifreeze protein from the longhorn sculpin, Myoxocephalus octodecimspinosis. Biochim Biophys Acta 1388(2):305–314CrossRefGoogle Scholar
  16. Deng G, Andrews DW, Laursen RA (1997) Amino acid sequence of a new type of antifreeze protein, from the longhorn sculpin Myoxocephalus octodecimspinosis. FEBS Lett 402(1):17–20CrossRefGoogle Scholar
  17. Desjardins M, Graham LA, Davies PL, Fletcher GL (2012) Antifreeze protein gene amplification facilitated niche exploitation and speciation in wolffish. FEBS J 279(12):2215–2230.  https://doi.org/10.1111/j.1742-4658.2012.08605.xCrossRefPubMedGoogle Scholar
  18. DeVries AL (1983) Antifreeze peptides and glycopeptides in cold-water fishes. Annu Rev Physiol 45:245–260.  https://doi.org/10.1146/annurev.ph.45.030183.001333CrossRefPubMedGoogle Scholar
  19. DeVries AL (1988) The role of antifreeze glycoproteins and peptides in the freezing avoidance of antarctic fishes. Comp Biochem Physiol B Biochem Mol Biol 90(3):611–621.  https://doi.org/10.1016/0305-0491(88)90302-1CrossRefGoogle Scholar
  20. DeVries AL, Komatsu SK, Feeney RE (1970) Chemical and physical properties of freezing point-depressing glycoproteins from Antarctic fishes. J Biol Chem 245(11):2901–2908PubMedGoogle Scholar
  21. Doucet D, Tyshenko MG, Davies PL, Walker VK (2002) A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. Eur J Biochem 269(1):38–46CrossRefGoogle Scholar
  22. Duman JG, Bennett V, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50(4):259–266.  https://doi.org/10.1016/j.jinsphys.2003.12.003CrossRefPubMedGoogle Scholar
  23. Ewart KV, Fletcher GL (1990) Isolation and characterization of antifreeze proteins from smelt (Osmerus-mordax) and atlantic herring (Clupea-harengus-harengus). Can J Zool Revue Can Zool 68(8):1652–1658.  https://doi.org/10.1139/z90-245CrossRefGoogle Scholar
  24. Fairley K, Westman BJ, Pham LH, Haymet AD, Harding MM, Mackay JP (2002) Type I shorthorn sculpin antifreeze protein: recombinant synthesis, solution conformation, and ice growth inhibition studies. J Biol Chem 277(27):24073–24080.  https://doi.org/10.1074/jbc.M200307200CrossRefPubMedGoogle Scholar
  25. Feeney RE (1974) A biological antifreeze. Am Sci 62(6):712–719PubMedGoogle Scholar
  26. Fletcher GL, Hew CL, Li X, Haya K, Kao MH (1985) Year-round presence of high levels of plasma antifreeze peptides in a temperate fish, ocean pout (Macrozoarces americanus). Can J Zool 63(3):488–493.  https://doi.org/10.1139/z85-070CrossRefGoogle Scholar
  27. Friis DS, Johnsen JL, Kristiansen E, Westh P, Ramløv H (2014a) Low thermodynamic but high kinetic stability of an antifreeze protein from Rhagium mordax. Protein Sci 23(6):760–768.  https://doi.org/10.1002/pro.2459CrossRefPubMedPubMedCentralGoogle Scholar
  28. Friis DS, Kristiansen E, von Solms N, Ramløv H (2014b) Antifreeze activity enhancement by site directed mutagenesis on an antifreeze protein from the beetle Rhagium mordax. FEBS Lett 588(9):1767–1772.  https://doi.org/10.1016/j.febslet.2014.03.032CrossRefPubMedGoogle Scholar
  29. García-Arribas O, Mateo R, Tomczak MM, Davies PL, Mateu MG (2007) Thermodynamic stability of a cold-adapted protein, type III antifreeze protein, and energetic contribution of salt bridges. Protein Sci 16(2):227–238.  https://doi.org/10.1110/ps.062448907CrossRefPubMedPubMedCentralGoogle Scholar
  30. Garnham CP, Campbell RL, Davies PL (2011) Anchored clathrate waters bind antifreeze proteins to ice. Proc Natl Acad Sci USA 108(18):7363–7367.  https://doi.org/10.1073/pnas.1100429108CrossRefPubMedGoogle Scholar
  31. Gauthier SY, Kay CM, Sykes BD, Walker VK, Davies PL (1998) Disulfide bond mapping and structural characterization of spruce budworm antifreeze protein. Eur J Biochem 258(2):445–453CrossRefGoogle Scholar
  32. Gauthier SY, Scotter AJ, Lin FH, Baardsnes J, Fletcher GL, Davies PL (2008) A re-evaluation of the role of type IV antifreeze protein. Cryobiology 57(3):292–296.  https://doi.org/10.1016/j.cryobiol.2008.10.122CrossRefPubMedGoogle Scholar
  33. Graham LA, Davies PL (2005) Glycine-rich antifreeze proteins from snow fleas. Science 310(5747):461.  https://doi.org/10.1126/science.1115145CrossRefPubMedGoogle Scholar
  34. Graham LA, Liou YC, Walker VK, Davies PL (1997) Hyperactive antifreeze protein from beetles. Nature 388(6644):727–728.  https://doi.org/10.1038/41908CrossRefPubMedGoogle Scholar
  35. Greenfield NJ (2006) Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat Protoc 1(6):2527–2535.  https://doi.org/10.1038/nprot.2006.204CrossRefPubMedPubMedCentralGoogle Scholar
  36. Gronwald W, Loewen MC, Lix B, Daugulis AJ, Sönnichsen FD, Davies PL, Sykes BD (1998) The solution structure of type II antifreeze protein reveals a new member of the lectin family. Biochemistry 37(14):4712–4721.  https://doi.org/10.1021/bi972788cCrossRefPubMedGoogle Scholar
  37. Hakim A, Nguyen JB, Basu K, Zhu DF, Thakral D, Davies PL, Isaacs FJ, Modis Y, Meng W (2013) Crystal structure of an insect antifreeze protein and its implications for ice binding. J Biol Chem 288(17):12295–12304.  https://doi.org/10.1074/jbc.M113.450973CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hew CL, Joshi S, Wang NC, Kao MH, Ananthanarayanan VS (1985) Structures of shorthorn sculpin antifreeze polypeptides. Eur J Biochem 151(1):167–172CrossRefGoogle Scholar
  39. Hew CL, Wang NC, Joshi S, Fletcher GL, Scott GK, Hayes PH, Buettner B, Davies PL (1988) Multiple genes provide the basis for antifreeze protein diversity and dosage in the ocean pout, Macrozoarces americanus. J Biol Chem 263(24):12049–12055PubMedGoogle Scholar
  40. Hobbs RS, Shears MA, Graham LA, Davies PL, Fletcher GL (2011) Isolation and characterization of type I antifreeze proteins from cunner, Tautogolabrus adspersus, order Perciformes. FEBS J 278(19):3699–3710.  https://doi.org/10.1111/j.1742-4658.2011.08288.xCrossRefPubMedGoogle Scholar
  41. Husby JA, Zachariassen KE (1980) Antifreeze agents in the body-fluid of winter active insects and spiders. Experientia 36(8):963–964.  https://doi.org/10.1007/bf01953821CrossRefGoogle Scholar
  42. Kao MH, Fletcher GL, Wang NC, Hew CL (1986) The relationship between molecular weight and antifreeze polypeptide activity in marine fish. Can J Zool Revue Can Zool 64(3):578–582.  https://doi.org/10.1139/z86-085CrossRefGoogle Scholar
  43. Kawahara H, Iwanaka Y, Higa S, Muryoi N, Sato M, Honda M, Omura H, Obata H (2007) A novel, intracellular antifreeze protein in an antarctic bacterium, Flavobacterium xanthum. Cryo Letters 28(1):39–49PubMedGoogle Scholar
  44. Ko TP, Robinson H, Gao YG, Cheng CH, DeVries AL, Wang AH (2003) The refined crystal structure of an eel pout type III antifreeze protein RD1 at 0.62-A resolution reveals structural microheterogeneity of protein and solvation. Biophys J 84(2 Pt 1):1228–1237.  https://doi.org/10.1016/S0006-3495(03)74938-8CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kristiansen E, Ramløv H, Hagen L, Pedersen SA, Andersen RA, Zachariassen KE (2005) Isolation and characterization of hemolymph antifreeze proteins from larvae of the longhorn beetle Rhagium inquisitor (L.). Comp Biochem Physiol B Biochem Mol Biol 142(1):90–97.  https://doi.org/10.1016/j.cbpc.2005.06.004CrossRefPubMedGoogle Scholar
  46. Kristiansen E, Pedersen SA, Zachariassen KE (2008) Salt-induced enhancement of antifreeze protein activity: a salting-out effect. Cryobiology 57(2):122–129.  https://doi.org/10.1016/j.cryobiol.2008.07.001CrossRefPubMedGoogle Scholar
  47. Kristiansen E, Wilkens C, Vincents B, Friis D, Lorentzen AB, Jenssen H, Løbner-Olesen A, Ramløv H (2012) Hyperactive antifreeze proteins from longhorn beetles: some structural insights. J Insect Physiol 58(11):1502–1510.  https://doi.org/10.1016/j.jinsphys.2012.09.004CrossRefPubMedGoogle Scholar
  48. Lee JK, Kim YJ, Park KS, Shin SC, Kim HJ, Song YH, Park H (2011) Molecular and comparative analyses of type IV antifreeze proteins (AFPIVs) from two Antarctic fishes, Pleuragramma antarcticum and Notothenia coriiceps. Comp Biochem Physiol B Biochem Mol Biol 159(4):197–205.  https://doi.org/10.1016/j.cbpb.2011.04.006CrossRefPubMedGoogle Scholar
  49. Leinala EK, Davies PL, Doucet D, Tyshenko MG, Walker VK, Jia Z (2002) A beta-helical antifreeze protein isoform with increased activity. Structural and functional insights. J Biol Chem 277(36):33349–33352.  https://doi.org/10.1074/jbc.M205575200CrossRefPubMedGoogle Scholar
  50. Li XM, Trinh KY, Hew CL (1991) Expression and characterization of an active and thermally more stable recombinant antifreeze polypeptide from ocean pout, Macrozoarces americanus, in Escherichia coli: improved expression by the modification of the secondary structure of the mRNA. Protein Eng 4(8):995–1002CrossRefGoogle Scholar
  51. Li N, Andorfer CA, Duman JG (1998a) Enhancement of insect antifreeze protein activity by solutes of low molecular mass. J Exp Biol 201(Pt 15):2243–2251PubMedGoogle Scholar
  52. Li N, Kendrick BS, Manning MC, Carpenter JF, Duman JG (1998b) Secondary structure of antifreeze proteins from overwintering larvae of the beetle Dendroides canadensis. Arch Biochem Biophys 360(1):25–32.  https://doi.org/10.1006/abbi.1998.0930CrossRefPubMedGoogle Scholar
  53. Lin X, O’Tousa JE, Duman JG (2010) Expression of two self-enhancing antifreeze proteins from the beetle Dendroides canadensis in Drosophila melanogaster. J Insect Physiol 56(4):341–349.  https://doi.org/10.1016/j.jinsphys.2009.11.005CrossRefPubMedGoogle Scholar
  54. Lin FH, Davies PL, Graham LA (2011) The Thr- and Ala-rich hyperactive antifreeze protein from inchworm folds as a flat silk-like β-helix. Biochemistry 50(21):4467–4478.  https://doi.org/10.1021/bi2003108CrossRefPubMedGoogle Scholar
  55. Liou YC, Thibault P, Walker VK, Davies PL, Graham LA (1999) A complex family of highly heterogeneous and internally repetitive hyperactive antifreeze proteins from the beetle Tenebrio molitor. Biochemistry 38(35):11415–11424.  https://doi.org/10.1021/bi990613sCrossRefPubMedGoogle Scholar
  56. Liou YC, Daley ME, Graham LA, Kay CM, Walker VK, Sykes BD, Davies PL (2000) Folding and structural characterization of highly disulfide-bonded beetle antifreeze protein produced in bacteria. Protein Expr Purif 19(1):148–157.  https://doi.org/10.1006/prep.2000.1219CrossRefPubMedPubMedCentralGoogle Scholar
  57. Liu Y, Li Z, Lin Q, Kosinski J, Seetharaman J, Bujnicki JM, Sivaraman J, Hew CL (2007) Structure and evolutionary origin of Ca(2+)-dependent herring type II antifreeze protein. PLoS One 2(6):e548.  https://doi.org/10.1371/journal.pone.0000548CrossRefPubMedPubMedCentralGoogle Scholar
  58. Lumry R, Eyring H (1954) Conformation changes of proteins. J Phys Chem 58(2):110–120.  https://doi.org/10.1021/j150512a005CrossRefGoogle Scholar
  59. Ma J, Wang J, Mao XF, Wang Y (2012) Differential expression of two antifreeze proteins in the desert beetle Anatolica polita (Coleoptera: Tenebriondae): seasonal variation and environmental effects. Cryo Letters 33(5):337–348PubMedGoogle Scholar
  60. Mao X, Liu Z, Li H, Ma J, Zhang F (2011) Calorimetric studies on an insect antifreeze protein ApAFP752 from Anatolica polita. J Therm Anal Calorim 104(1):343–349.  https://doi.org/10.1007/s10973-010-1067-3CrossRefGoogle Scholar
  61. Marshall CB, Daley ME, Sykes BD, Davies PL (2004a) Enhancing the activity of a beta-helical antifreeze protein by the engineered addition of coils. Biochemistry 43(37):11637–11646.  https://doi.org/10.1021/bi0488909CrossRefPubMedGoogle Scholar
  62. Marshall CB, Fletcher GL, Davies PL (2004b) Hyperactive antifreeze protein in a fish. Nature 429(6988):153.  https://doi.org/10.1038/429153aCrossRefPubMedGoogle Scholar
  63. Marshall CB, Chakrabartty A, Davies PL (2005) Hyperactive antifreeze protein from winter flounder is a very long rod-like dimer of alpha-helices. J Biol Chem 280(18):17920–17929.  https://doi.org/10.1074/jbc.M500622200CrossRefPubMedGoogle Scholar
  64. Miura K, Ohgiya S, Hoshino T, Nemoto N, Suetake T, Miura A, Spyracopoulos L, Kondo H, Tsuda S (2001) NMR analysis of type III antifreeze protein intramolecular dimer. Structural basis for enhanced activity. J Biol Chem 276(2):1304–1310.  https://doi.org/10.1074/jbc.M007902200CrossRefPubMedGoogle Scholar
  65. Mok YF, Lin FH, Graham LA, Celik Y, Braslavsky I, Davies PL (2010) Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry 49(11):2593–2603.  https://doi.org/10.1021/bi901929nCrossRefPubMedGoogle Scholar
  66. Neelakanta G, Sultana H, Fish D, Anderson JF, Fikrig E (2010) Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. J Clin Invest 120(9):3179–3190.  https://doi.org/10.1172/JCI42868CrossRefPubMedPubMedCentralGoogle Scholar
  67. 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(Pt 9):1695–1703.  https://doi.org/10.1242/jeb.082461CrossRefPubMedGoogle Scholar
  68. Nishimiya Y, Kondo H, Takamichi M, Sugimoto H, Suzuki M, Miura A, Tsuda S (2008) Crystal structure and mutational analysis of Ca2+−independent type II antifreeze protein from longsnout poacher, Brachyopsis rostratus. J Mol Biol 382(3):734–746.  https://doi.org/10.1016/j.jmb.2008.07.042CrossRefPubMedGoogle Scholar
  69. Qiu LM, Ma J, Wang J, Zhang FC, Wang Y (2010a) Thermal stability properties of an antifreeze protein from the desert beetle Microdera punctipennis. Cryobiology 60(2):192–197.  https://doi.org/10.1016/j.cryobiol.2009.10.014CrossRefPubMedGoogle Scholar
  70. Qiu L, Wang Y, Wang J, Zhang F, Ma J (2010b) Expression of biologically active recombinant antifreeze protein His-MpAFP149 from the desert beetle (Microdera punctipennis dzungarica) in Escherichia coli. Mol Biol Rep 37(4):1725–1732.  https://doi.org/10.1007/s11033-009-9594-3CrossRefPubMedGoogle Scholar
  71. Salvay AG, Santos J, Howard EI (2007) Electro-optical properties characterization of fish type III antifreeze protein. J Biol Phys 33(5-6):389–397.  https://doi.org/10.1007/s10867-008-9080-5CrossRefPubMedGoogle Scholar
  72. Sanchez-Ruiz JM (2010) Protein kinetic stability. Biophys Chem 148(1–3):1–15.  https://doi.org/10.1016/j.bpc.2010.02.004CrossRefPubMedGoogle Scholar
  73. Scott GK, Davies PL, Shears MA, Fletcher GL (1987) Structural variations in the alanine-rich antifreeze proteins of the pleuronectinae. Eur J Biochem 168(3):629–633CrossRefGoogle Scholar
  74. Scott GK, Hayes PH, Fletcher GL, Davies PL (1988) Wolffish antifreeze protein genes are primarily organized as tandem repeats that each contain two genes in inverted orientation. Mol Cell Biol 8(9):3670–3675CrossRefGoogle Scholar
  75. Slaughter D, Fletcher GL, Ananthanarayanan VS, Hew CL (1981) Antifreeze proteins from the sea raven, Hemitripterus americanus. Further evidence for diversity among fish polypeptide antifreezes. J Biol Chem 256(4):2022–2026PubMedGoogle Scholar
  76. Sönnichsen FD, Sykes BD, Chao H, Davies PL (1993) The nonhelical structure of antifreeze protein type III. Science 259(5098):1154–1157CrossRefGoogle Scholar
  77. Sönnichsen FD, Sykes BD, Davies PL (1995) Comparative modeling of the three-dimensional structure of type II antifreeze protein. Protein Sci 4(3):460–471.  https://doi.org/10.1002/pro.5560040313CrossRefPubMedPubMedCentralGoogle Scholar
  78. Sönnichsen FD, DeLuca CI, Davies PL, Sykes BD (1996) Refined solution structure of type III antifreeze protein: hydrophobic groups may be involved in the energetics of the protein-ice interaction. Structure 4(11):1325–1337CrossRefGoogle Scholar
  79. Sørensen TF, Cheng CH, Ramløv H (2006) Isolation and some characterisation of antifreeze protein from the European eelpout Zoarces viviparus. Cryo Letters 27(6):387–399PubMedGoogle Scholar
  80. Sun T, Lin FH, Campbell RL, Allingham JS, Davies PL (2014) An antifreeze protein folds with an interior network of more than 400 semi-clathrate waters. Science 343(6172):795–798.  https://doi.org/10.1126/science.1247407CrossRefPubMedGoogle Scholar
  81. Tursman D, Duman JG (1995) Cryoprotective effects of thermal hysteresisprotein on survivorship of frozen gut cells from the freeze-tolerant centipede Lithobius forficatus. J Exp Zool 272(4):249–257.  https://doi.org/10.1002/jez.1402720402CrossRefGoogle Scholar
  82. Venketesh S, Dayananda C (2008) Properties, potentials, and prospects of antifreeze proteins. Crit Rev Biotechnol 28(1):57–82.  https://doi.org/10.1080/07388550801891152CrossRefPubMedGoogle Scholar
  83. Wang L, Duman JG (2005) Antifreeze proteins of the beetle Dendroides canadensis enhance one another’s activities. Biochemistry 44(30):10305–10312.  https://doi.org/10.1021/bi050728yCrossRefPubMedGoogle Scholar
  84. Wang X, DeVries AL, Cheng CH (1995) Antifreeze peptide heterogeneity in an antarctic eel pout includes an unusually large major variant comprised of two 7 kDa type III AFPs linked in tandem. Biochim Biophys Acta 1247(2):163–172CrossRefGoogle Scholar
  85. Wang C, Oliver EE, Christner BC, Luo BH (2016) Functional analysis of a bacterial antifreeze protein indicates a cooperative effect between its two ice-binding domains. Biochemistry 55(28):3975–3983.  https://doi.org/10.1021/acs.biochem.6b00323CrossRefPubMedGoogle Scholar
  86. Wilkens C, Poulsen JC, Ramløv H, Lo Leggio L (2014) Purification, crystal structure determination and functional characterization of type III antifreeze proteins from the European eelpout Zoarces viviparus. Cryobiology 69(1):163–168.  https://doi.org/10.1016/j.cryobiol.2014.07.003CrossRefPubMedGoogle Scholar
  87. Wu DW, Duman JG, Cheng C-HC, Castellino FJ (1991) Purification and characterization of antifreeze proteins from larvae of the beetle Dendroides canadensis. J Comp Physiol B 161(3):271–278.  https://doi.org/10.1007/BF00262308CrossRefGoogle Scholar
  88. Wu Y, Banoub J, Goddard SV, Kao MH, Fletcher GL (2001) Antifreeze glycoproteins: relationship between molecular weight, thermal hysteresis and the inhibition of leakage from liposomes during thermotropic phase transition. Comp Biochem Physiol B Biochem Mol Biol 128(2):265–273CrossRefGoogle Scholar
  89. Yamashita Y, Miura R, Takemoto Y, Tsuda S, Kawahara H, Obata H (2003) Type II antifreeze protein from a mid-latitude freshwater fish, Japanese smelt (Hypomesus nipponensis). Biosci Biotechnol Biochem 67(3):461–466CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Dennis Steven Friis
    • 1
  • Hans Ramløv
    • 2
  1. 1.CopenhagenDenmark
  2. 2.Department of Natural SciencesRoskilde UniversityRoskildeDenmark

Personalised recommendations