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Mutational Studies on Antifreeze Proteins

  • Dennis Steven Friis
  • Hans Ramløv
Chapter
  • 11 Downloads

Abstract

When investigating proteins, the possibility of introducing targeted changes and observing their effect can be a useful tool. In regard to antifreeze proteins, this possibility has given rise to various kinds of studies. The method of observing which specific planes on the ice crystal the different antifreeze proteins bind to has been improved by fusing antifreeze proteins to fluorescent proteins. It has also provided insight into whether the antifreeze proteins bind to ice irreversibly or not, by microfluidic experiments. Using site-directed mutagenesis it has been studied how different amino acid side chains, and more specifically their functional groups, affect the interaction with ice. These studies led to a change in the perception that hydrogen bonds were the key force driving the interaction, to believing that the hydrophobic or van der Waals forces are dominant in this regard. It has also been achieved to increase the activity of antifreeze proteins, and though much is still to be learned about the antifreeze proteins, the future mutagenic studies could very well be focusing on optimising the proteins. This could be relevant, not only in regard to activity, but also in the general tailoring of the protein to specific purposes, in order to make the protein relevant for specific commercial respects in the future.

Keywords

Site-directed mutagenesis Ice-binding domain Amino acid Threonine Substitution Side chain Functional groups Fusion protein Ice interaction 

References

  1. Baardsnes J, Kondejewski LH, Hodges RS, Chao H, Kay C, Davies PL (1999) New ice-binding face for type I antifreeze protein. FEBS Lett 463(1–2):87–91CrossRefGoogle Scholar
  2. Baardsnes J, Jelokhani-Niaraki M, Kondejewski LH, Kuiper MJ, Kay CM, Hodges RS, Davies PL (2001) Antifreeze protein from shorthorn sculpin: identification of the ice-binding surface. Protein Sci 10(12):2566–2576.  https://doi.org/10.1110/ps.ps.26501CrossRefPubMedPubMedCentralGoogle Scholar
  3. Baardsnes J, Kuiper MJ, Davies PL (2003) Antifreeze protein dimer: when two ice-binding faces are better than one. J Biol Chem 278(40):38942–38947.  https://doi.org/10.1074/jbc.M306776200CrossRefPubMedGoogle Scholar
  4. Bagis H, Aktoprakligil D, Mercan HO, Yurdusev N, Turgut G, Sekmen S, Arat S, Cetin S (2006) Stable transmission and transcription of newfoundland ocean pout type III fish antifreeze protein (AFP) gene in transgenic mice and hypothermic storage of transgenic ovary and testis. Mol Reprod Dev 73(11):1404–1411.  https://doi.org/10.1002/mrd.20601CrossRefPubMedGoogle Scholar
  5. Bagis H, Akkoc T, Tass A, Aktoprakligil D (2008) Cryogenic effect of antifreeze protein on transgenic mouse ovaries and the production of live offspring by orthotopic transplantation of cryopreserved mouse ovaries. Mol Reprod Dev 75(4):608–613.  https://doi.org/10.1002/mrd.20799CrossRefPubMedGoogle Scholar
  6. Bang JK, Lee JH, Murugan RN, Lee SG, Do H, Koh HY, Shim HE, Kim HC, Kim HJ (2013) Antifreeze peptides and glycopeptides, and their derivatives: potential uses in biotechnology. Mar Drugs 11(6):2013–2041.  https://doi.org/10.3390/md11062013CrossRefPubMedPubMedCentralGoogle Scholar
  7. Basu K, Garnham CP, Nishimiya Y, Tsuda S, Braslavsky I, Davies P (2014) Determining the ice-binding planes of antifreeze proteins by fluorescence-based ice plane affinity. J Vis Exp 83:e51185.  https://doi.org/10.3791/51185CrossRefGoogle Scholar
  8. 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
  9. Bredow M, Walker VK (2017) Ice-binding proteins in plants. Front Plant Sci 8:2153–2153.  https://doi.org/10.3389/fpls.2017.02153CrossRefPubMedPubMedCentralGoogle Scholar
  10. Celik Y, Drori R, Pertaya-Braun N, Altan A, Barton T, Bar-Dolev M, Groisman A, Davies PL, Braslavsky I (2013) Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth. Proc Natl Acad Sci U S A 110(4):1309–1314.  https://doi.org/10.1073/pnas.1213603110CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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
  12. 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
  13. Chao H, Houston ME, Hodges RS, Kay CM, Sykes BD, Loewen MC, Davies PL, Sönnichsen FD (1997) A diminished role for hydrogen bonds in antifreeze protein binding to ice. Biochemistry 36(48):14652–14660.  https://doi.org/10.1021/bi970817dCrossRefPubMedGoogle Scholar
  14. DeLuca CI, Chao H, Sönnichsen FD, Sykes BD, Davies PL (1996) Effect of type III antifreeze protein dilution and mutation on the growth inhibition of ice. Biophys J 71(5):2346–2355.  https://doi.org/10.1016/S0006-3495(96)79476-6CrossRefPubMedPubMedCentralGoogle Scholar
  15. DeLuca CI, Comley R, Davies PL (1998a) Antifreeze proteins bind independently to ice. Biophys J 74(3):1502–1508.  https://doi.org/10.1016/S0006-3495(98)77862-2CrossRefPubMedPubMedCentralGoogle Scholar
  16. DeLuca CI, Davies PL, Ye Q, Jia Z (1998b) The effects of steric mutations on the structure of type III antifreeze protein and its interaction with ice. J Mol Biol 275(3):515–525.  https://doi.org/10.1006/jmbi.1997.1482CrossRefPubMedGoogle Scholar
  17. Devries AL, Lin Y (1977) Structure of a peptide antifreeze and mechanism of adsorption to ice. Biochim Biophys Acta 495(2):388–392CrossRefGoogle Scholar
  18. Doucet D, Tyshenko MG, Kuiper MJ, Graether SP, Sykes BD, Daugulis AJ, Davies PL, Walker VK (2000) Structure-function relationships in spruce budworm antifreeze protein revealed by isoform diversity. Eur J Biochem 267(19):6082–6088CrossRefGoogle Scholar
  19. Duncker BP, Chen CP, Davies PL, Walker VK (1995) Antifreeze protein does not confer cold tolerance to transgenic Drosophila melanogaster. Cryobiology 32(6):521–527.  https://doi.org/10.1006/cryo.1995.1054CrossRefPubMedGoogle Scholar
  20. Ebbinghaus S, Meister K, Prigozhin MB, Devries AL, Havenith M, Dzubiella J, Gruebele M (2012) Functional importance of short-range binding and long-range solvent interactions in helical antifreeze peptides. Biophys J 103(2):L20–L22.  https://doi.org/10.1016/j.bpj.2012.06.013CrossRefPubMedPubMedCentralGoogle Scholar
  21. Ewart KV, Fletcher GL (1993) Herring antifreeze protein: primary structure and evidence for a C-type lectin evolutionary origin. Mol Mar Biol Biotechnol 2(1):20–27PubMedGoogle Scholar
  22. Ewart KV, Rubinsky B, Fletcher GL (1992) Structural and functional similarity between fish antifreeze proteins and calcium-dependent lectins. Biochem Biophys Res Commun 185(1):335–340CrossRefGoogle Scholar
  23. Ewart KV, Li Z, Yang DS, Fletcher GL, Hew CL (1998) The ice-binding site of Atlantic herring antifreeze protein corresponds to the carbohydrate-binding site of C-type lectins. Biochemistry 37(12):4080–4085.  https://doi.org/10.1021/bi972503wCrossRefPubMedGoogle Scholar
  24. Friis DS, Kristiansen E, von Solms N, Ramløv H (2014) 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
  25. Garnham CP, Natarajan A, Middleton AJ, Kuiper MJ, Braslavsky I, Davies PL (2010) Compound ice-binding site of an antifreeze protein revealed by mutagenesis and fluorescent tagging. Biochemistry 49(42):9063–9071.  https://doi.org/10.1021/bi100516eCrossRefPubMedGoogle Scholar
  26. Graether SP, Kuiper MJ, Gagné SM, Walker VK, Jia Z, Sykes BD, Davies PL (2000) Beta-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature 406(6793):325–328.  https://doi.org/10.1038/35018610CrossRefPubMedGoogle Scholar
  27. Gwak Y, Jung W, Lee Y, Kim JS, Kim CG, Ju JH, Song C, Hyun JK, Jin E (2014) An intracellular antifreeze protein from an Antarctic microalga that responds to various environmental stresses. FASEB J 28(11):4924–4935.  https://doi.org/10.1096/fj.14-256388CrossRefPubMedGoogle Scholar
  28. Haymet AD, Ward LG, Harding MM, Knight CA (1998) Valine substituted winter flounder ‘antifreeze’: preservation of ice growth hysteresis. FEBS Lett 430(3):301–306CrossRefGoogle Scholar
  29. Haymet ADJ, Ward LG, Harding MM (1999) Winter flounder “antifreeze” proteins: synthesis and ice growth inhibition of analogues that probe the relative importance of hydrophobic and hydrogen-bonding interactions. J Am Chem Soc 121(5):941–948.  https://doi.org/10.1021/ja9801341CrossRefGoogle Scholar
  30. Haymet AD, Ward LG, Harding MM (2001) Hydrophobic analogues of the winter flounder ‘antifreeze’ protein. FEBS Lett 491(3):285–288CrossRefGoogle Scholar
  31. Hays LM, Feeney RE, Crowe LM, Crowe JH, Oliver AE (1996) Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic phase transitions. Proc Natl Acad Sci U S A 93(13):6835–6840CrossRefGoogle Scholar
  32. Heisig M, Mattessich S, Rembisz A, Acar A, Shapiro M, Booth CJ, Neelakanta G, Fikrig E (2015) Frostbite protection in mice expressing an antifreeze glycoprotein. PLoS One 10(2):e0116562.  https://doi.org/10.1371/journal.pone.0116562CrossRefPubMedPubMedCentralGoogle Scholar
  33. Holmberg N, Lilius G, Bulow L (1994) Artificial antifreeze proteins can improve NaCl tolerance when expressed in E. coli. FEBS Lett 349(3):354–358CrossRefGoogle Scholar
  34. Huang T, Nicodemus J, Zarka DG, Thomashow MF, Wisniewski M, Duman JG (2002) Expression of an insect (Dendroides canadensis) antifreeze protein in Arabidopsis thaliana results in a decrease in plant freezing temperature. Plant Mol Biol 50(3):333–344CrossRefGoogle Scholar
  35. Jiang M, Ma J, Qiu LM (2011) Cryoprotective effect of an insect antifreeze protein MpAFP 698 and its mutants from the desert beetle Microdera punctipennis. Cryo Letters 32(5):436–446PubMedGoogle Scholar
  36. Jorgensen WL, Tirado-Rives J (1988) The OPLS potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin. J Am Chem Soc 110(6):1657–1666.  https://doi.org/10.1021/ja00214a001CrossRefPubMedGoogle Scholar
  37. Kenward KD, Brandle J, McPherson J, Davies PL (1999) Type II fish antifreeze protein accumulation in transgenic tobacco does not confer frost resistance. Transgenic Res 8(2):105–117.  https://doi.org/10.1023/A:100888662CrossRefPubMedGoogle Scholar
  38. Kim H-E, Lee A-R, Lee Y-M, Jeong M, Park C-J, Lee J-H (2013) Hydrogen exchange study of winter flounder type I antifreeze protein. Bull Kor Chem Soc 34(10):3137–3140CrossRefGoogle Scholar
  39. Knight CA, Cheng CC, DeVries AL (1991) Adsorption of alpha-helical antifreeze peptides on specific ice crystal surface planes. Biophys J 59(2):409–418.  https://doi.org/10.1016/S0006-3495(91)82234-2CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kondo H, Hanada Y, Sugimoto H, Hoshino T, Garnham CP, Davies PL, Tsuda S (2012) Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation. Proc Natl Acad Sci U S A 109(24):9360–9365.  https://doi.org/10.1073/pnas.1121607109CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kristiansen E, Ramløv H, Højrup 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(2):109–117.  https://doi.org/10.1016/j.ibmb.2010.11.002CrossRefPubMedGoogle Scholar
  42. 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
  43. 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
  44. 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
  45. Li Z, Lin Q, Yang DS, Ewart KV, Hew CL (2004) The role of Ca2+-coordinating residues of herring antifreeze protein in antifreeze activity. Biochemistry 43(46):14547–14554.  https://doi.org/10.1021/bi048485hCrossRefPubMedGoogle Scholar
  46. 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
  47. 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
  48. 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
  49. Liu K, Jia Z, Chen G, Tung C, Liu R (2005) Systematic size study of an insect antifreeze protein and its interaction with ice. Biophys J 88(2):953–958.  https://doi.org/10.1529/biophysj.104.051169CrossRefPubMedPubMedCentralGoogle Scholar
  50. Loewen MC, Gronwald W, Sönnichsen FD, Sykes BD, Davies PL (1998) The ice-binding site of sea raven antifreeze protein is distinct from the carbohydrate-binding site of the homologous C-type lectin. Biochemistry 37(51):17745–17753CrossRefGoogle Scholar
  51. Loewen MC, Chao H, Houston ME, Baardsnes J, Hodges RS, Kay CM, Sykes BD, Sönnichsen FD, Davies PL (1999) Alternative roles for putative ice-binding residues in type I antifreeze protein. Biochemistry 38(15):4743–4749.  https://doi.org/10.1021/bi982602pCrossRefPubMedGoogle Scholar
  52. Mao X, Liu Z, Ma J, Pang H, Zhang F (2011) Characterization of a novel β-helix antifreeze protein from the desert beetle Anatolica polita. Cryobiology 62(2):91–99.  https://doi.org/10.1016/j.cryobiol.2011.01.001CrossRefPubMedGoogle Scholar
  53. Marshall CB, Daley ME, Graham LA, Sykes BD, Davies PL (2002) Identification of the ice-binding face of antifreeze protein from Tenebrio molitor. FEBS Lett 529(2-3):261–267CrossRefGoogle Scholar
  54. Marshall CB, Daley ME, Sykes BD, Davies PL (2004) 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/bi0488909.CrossRefPubMedGoogle Scholar
  55. McKown RL, Warren GJ (1991) Enhanced survival of yeast expressing an antifreeze gene analogue after freezing. Cryobiology 28(5):474–482CrossRefGoogle Scholar
  56. Meijer PJ, Holmberg N, Grundstrom G, Bulow L (1996) Directed evolution of a type I antifreeze protein expressed in Escherichia coli with sodium chloride as selective pressure and its effect on antifreeze tolerance. Protein Eng 9(11):1051–1054CrossRefGoogle Scholar
  57. Middleton AJ, Brown AM, Davies PL, Walker VK (2009) Identification of the ice-binding face of a plant antifreeze protein. FEBS Lett 583(4):815–819.  https://doi.org/10.1016/j.febslet.2009.01.035CrossRefPubMedGoogle Scholar
  58. 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
  59. Neelakanta G, Hudson AM, Sultana H, Cooley L, Fikrig E (2012) Expression of Ixodes scapularis antifreeze glycoprotein enhances cold tolerance in Drosophila melanogaster. PLoS One 7(3):e33447.  https://doi.org/10.1371/journal.pone.0033447CrossRefPubMedPubMedCentralGoogle Scholar
  60. Nishimiya Y, Ohgiya S, Tsuda S (2003) Artificial multimers of the type III antifreeze protein. Effects on thermal hysteresis and ice crystal morphology. J Biol Chem 278(34):32307–32312.  https://doi.org/10.1074/jbc.M304390200CrossRefPubMedGoogle Scholar
  61. 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
  62. Panadero J, Randez-Gil F, Prieto JA (2005) Heterologous expression of type I antifreeze peptide GS-5 in baker’s yeast increases freeze tolerance and provides enhanced gas production in frozen dough. J Agric Food Chem 53(26):9966–9970.  https://doi.org/10.1021/jf0515577CrossRefPubMedGoogle Scholar
  63. Pertaya N, Marshall CB, DiPrinzio CL, Wilen L, Thomson ES, Wettlaufer JS, Davies PL, Braslavsky I (2007) Fluorescence microscopy evidence for quasi-permanent attachment of antifreeze proteins to ice surfaces. Biophys J 92(10):3663–3673.  https://doi.org/10.1529/biophysj.106.096297CrossRefPubMedPubMedCentralGoogle Scholar
  64. Pertaya N, Marshall CB, Celik Y, Davies PL, Braslavsky I (2008) Direct visualization of spruce budworm antifreeze protein interacting with ice crystals: basal plane affinity confers hyperactivity. Biophys J 95(1):333–341.  https://doi.org/10.1529/biophysj.107.125328CrossRefPubMedPubMedCentralGoogle Scholar
  65. Provencher SW, Glöckner J (1981) Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20(1):33–37CrossRefGoogle Scholar
  66. 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
  67. 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
  68. Rubinsky B, Arav A, Mattioli M, Devries AL (1990) The effect of antifreeze glycopeptides on membrane potential changes at hypothermic temperatures. Biochem Biophys Res Commun 173(3):1369–1374CrossRefGoogle Scholar
  69. Sicheri F, Yang DS (1995) Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature 375(6530):427–431.  https://doi.org/10.1038/375427a0CrossRefPubMedGoogle Scholar
  70. 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
  71. Stevens CA, Drori R, Zalis S, Braslavsky I, Davies PL (2015) Dendrimer-linked antifreeze proteins have superior activity and thermal recovery. Bioconjug Chem 26(9):1908–1915.  https://doi.org/10.1021/acs.bioconjchem.5b00290CrossRefPubMedGoogle Scholar
  72. Tablin F, Oliver AE, Walker NJ, Crowe LM, Crowe JH (1996) Membrane phase transition of intact human platelets: correlation with cold-induced activation. J Cell Physiol 168(2):305–313.  https://doi.org/10.1002/(sici)1097-4652(199608)168:2<305::aid-jcp9>3.0.co;2-tCrossRefPubMedGoogle Scholar
  73. Tomczak MM, Hincha DK, Estrada SD, Feeney RE, Crowe JH (2001) Antifreeze proteins differentially affect model membranes during freezing. Biochim Biophys Acta 1511(2):255–263CrossRefGoogle Scholar
  74. Tomczak MM, Hincha DK, Estrada SD, Wolkers WF, Crowe LM, Feeney RE, Tablin F, Crowe JH (2002) A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophys J 82(2):874–881.  https://doi.org/10.1016/s0006-3495(02)75449-0CrossRefPubMedPubMedCentralGoogle Scholar
  75. Tyshenko MG, Walker VK (2004) Hyperactive spruce budworm antifreeze protein expression in transgenic Drosophila does not confer cold shock tolerance. Cryobiology 49(1):28–36.  https://doi.org/10.1016/j.cryobiol.2004.04.002CrossRefPubMedGoogle Scholar
  76. 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
  77. Wang Y, Qiu L, Dai C, Wang J, Luo J, Zhang F, Ma J (2008) Expression of insect (Microdera puntipennis dzungarica) antifreeze protein MpAFP149 confers the cold tolerance to transgenic tobacco. Plant Cell Rep 27(8):1349–1358.  https://doi.org/10.1007/s00299-008-0562-5CrossRefPubMedGoogle Scholar
  78. Wen D, Laursen RA (1992) Structure-function relationships in an antifreeze polypeptide. The role of neutral, polar amino acids. J Biol Chem 267(20):14102–14108PubMedGoogle Scholar
  79. Wen D, Laursen RA (1993a) A D-antifreeze polypeptide displays the same activity as its natural L-enantiomer. FEBS Lett 317(1-2):31–34CrossRefGoogle Scholar
  80. Wen D, Laursen RA (1993b) Structure-function relationships in an antifreeze polypeptide. The effect of added bulky groups on activity. J Biol Chem 268(22):16401–16405PubMedGoogle Scholar
  81. Wen D, Laursen RA (1993c) Structure-function relationships in an antifreeze polypeptide. The role of charged amino acids. J Biol Chem 268(22):16396–16400PubMedGoogle Scholar
  82. Zepeda S, Yokoyama E, Uda Y, Katagiri C, Furukawa Y (2008) Situ observation of antifreeze glycoprotein kinetics at the ice interface reveals a two-step reversible adsorption mechanism. Cryst Growth Des 8(10):3666–3672.  https://doi.org/10.1021/cg800269wCrossRefGoogle Scholar
  83. Zhang W, Laursen RA (1998) Structure-function relationships in a type I antifreeze polypeptide. The role of threonine methyl and hydroxyl groups in antifreeze activity. J Biol Chem 273(52):34806–34812CrossRefGoogle Scholar
  84. Zhang L, Jin Q, Luo J, Wu J, Wang S, Wang Z, Gong S, Zhang W, Lan X (2018) Intracellular expression of antifreeze peptides in food grade lactococcus lactis and evaluation of their cryoprotective activity. J Food Sci 83(5):1311–1320.  https://doi.org/10.1111/1750-3841.14117CrossRefPubMedGoogle 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

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