1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biochemistry
  4. Volume 85, 2016
  5. Article

Annual Review of Biochemistry

Volume 85, 2016

Ice-Binding Proteins and Their Function

Abstract

Ice-binding proteins (IBPs) are a diverse class of proteins that assist organism survival in the presence of ice in cold climates. They have different origins in many organisms, including bacteria, fungi, algae, diatoms, plants, insects, and fish. This review covers the gamut of IBP structures and functions and the common features they use to bind ice. We discuss mechanisms by which IBPs adsorb to ice and interfere with its growth, evidence for their irreversible association with ice, and methods for enhancing the activity of IBPs. The applications of IBPs in the food industry, in cryopreservation, and in other technologies are vast, and we chart out some possibilities.

Keyword(s): anchored clathrate waters, antifreeze proteins, ice-binding site, ice-structuring proteins, thermal hysteresis
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-060815-014546
2016-06-02
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/biochem/85/1/annurev-biochem-060815-014546.html?itemId=/content/journals/10.1146/annurev-biochem-060815-014546&mimeType=html&fmt=ahah

Literature Cited

  1. DeVries AL, Komatsu SK, Feeney RE. 1.  1970. Purification and characterization of a freezing-point-depressant glycoprotein from Antarctic fish. J. Biol. Chem. 245:2901–8 [Google Scholar]
  2. DeVries AL, Wohlschlag DE. 2.  1969. Freezing resistance in some Antarctic fishes. Science 163:1073–75 [Google Scholar]
  3. Davies PL. 3.  2014. Ice-binding proteins: a remarkable diversity of structures for stopping and starting ice growth. Trends Biochem. Sci. 39:548–55 [Google Scholar]
  4. Duman JG, Patterson JL. 4.  1978. Role of thermal-hysteresis-proteins in low-temperature tolerance of insects and spiders. Cryobiology 15:683–84 [Google Scholar]
  5. Urrutia ME, Duman JG, Knight CA. 5.  1992. Plant thermal hysteresis proteins. Biochim. Biophys. Acta 1121:199–206 [Google Scholar]
  6. Meyer K, Keil M, Naldrett MJ. 6.  1999. A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Lett. 447:171–78 [Google Scholar]
  7. Guo S, Garnham CP, Whitney JC, Graham LA, Davies PL. 7.  2012. Re-evaluation of a bacterial antifreeze protein as an adhesin with ice-binding activity. PLOS ONE 7:e48805 [Google Scholar]
  8. Clarke CJ, Buckley SL, Lindner N. 8.  2002. Ice structuring proteins—a new name for antifreeze proteins. CryoLetters 23:89–92 [Google Scholar]
  9. Raymond JA, DeVries AL. 9.  1977. Adsorption inhibition as a mechanism of freezing resistance in polar fishes. PNAS 74:2589–93 [Google Scholar]
  10. Knight CA, DeVries AL. 10.  2009. Ice growth in supercooled solutions of a biological “antifreeze,” AFGP 1–5: an explanation in terms of adsorption rate for the concentration dependence of the freezing point. Phys. Chem. Chem. Phys. 11:5749–61 [Google Scholar]
  11. Drori R, Davies PL, Braslavsky I. 11.  2015. When are antifreeze proteins in solution essential for ice growth inhibition?. Langmuir 31:5805–11 [Google Scholar]
  12. Celik Y, Drori R, Pertaya-Braun N, Altan A, Barton T. 12.  et al. 2013. Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth. PNAS 110:1309–14 [Google Scholar]
  13. Duman JG. 13.  2015. Animal ice-binding (antifreeze) proteins and glycolipids: an overview with emphasis on physiological function. J. Exp. Biol. 218:1846–55 [Google Scholar]
  14. Venketesh S, Dayananda C. 14.  2008. Properties, potentials, and prospects of antifreeze proteins. Crit. Rev. Biotechnol. 28:57–82 [Google Scholar]
  15. Wilson SL, Kelley DL, Walker VK. 15.  2006. Ice-active characteristics of soil bacteria selected by ice-affinity. Environ. Microbiol. 8:1816–24 [Google Scholar]
  16. Sander LM, Tkachenko AV. 16.  2004. Kinetic pinning and biological antifreezes. Phys. Rev. Lett. 93:128102 [Google Scholar]
  17. Knight CA, DeVries AL, Oolman LD. 17.  1984. Fish antifreeze protein and the freezing and recrystallization of ice. Nature 308:295–96 [Google Scholar]
  18. Gauthier SY, Scotter AJ, Lin FH, Baardsnes J, Fletcher GL, Davies PL. 18.  2008. A re-evaluation of the role of type IV antifreeze protein. Cryobiology 57:292–96 [Google Scholar]
  19. Knight CA. 19.  2000. Structural biology: adding to the antifreeze agenda. Nature 406:249–51 [Google Scholar]
  20. Bar-Dolev M, Celik Y, Wettlaufer JS, Davies PL, Braslavsky I. 20.  2012. New insights into ice growth and melting modifications by antifreeze proteins. J. R. Soc. Interface 9:3249–59 [Google Scholar]
  21. Jeong JS, Ansaloni A, Mezzenga R, Lashuel HA, Dietler G. 21.  2013. Novel mechanistic insight into the molecular basis of amyloid polymorphism and secondary nucleation during amyloid formation. J. Mol. Biol. 425:101765–81 [Google Scholar]
  22. Kiani H, Sun DW. 22.  2011. Water crystallization and its importance to freezing of foods: a review. Trends Food Sci. Technol. 22:407–26 [Google Scholar]
  23. Celik Y, Graham LA, Mok YF, Bar M, Davies PL, Braslavsky I. 23.  2010. Superheating of ice crystals in antifreeze protein solutions. PNAS 107:5423–28 [Google Scholar]
  24. Knight CA, DeVries AL. 24.  1989. Melting inhibition and superheating of ice by an antifreeze glycopeptide. Science 245:505–7 [Google Scholar]
  25. Cziko PA, DeVries AL, Evans CW, Cheng C-HC. 25.  2014. Antifreeze protein-induced superheating of ice inside Antarctic notothenioid fishes inhibits melting during summer warming. PNAS 111:14583–88 [Google Scholar]
  26. Braslavsky I, Drori R. 26.  2013. LabVIEW-operated novel nanoliter osmometer for ice binding protein investigations. J. Vis. Exp. 72:4189 [Google Scholar]
  27. Inada T, Lu S-S. 27.  2004. Thermal hysteresis caused by non-equilibrium antifreeze activity of poly(vinyl alcohol). Chem. Phys. Lett. 394:361–65 [Google Scholar]
  28. Amornwittawat N, Wang S, Duman JG, Wen X. 28.  2008. Polycarboxylates enhance beetle antifreeze protein activity. Biochim. Biophys. Acta 1784:1942–48 [Google Scholar]
  29. Scholander PF, van Dam L, Kanwisher JW, Hammel HT, Gordon MS. 29.  1957. Supercooling and osmoregulation in arctic fish. J. Cell. Comp. Physiol. 49:5–24 [Google Scholar]
  30. Duman JG, Bennett V, Sformo T, Hochstrasser R, Barnes BM. 30.  2004. Antifreeze proteins in Alaskan insects and spiders. J. Insect Physiol. 50:259–66 [Google Scholar]
  31. Graham LA, Liou YC, Walker VK, Davies PL. 31.  1997. Hyperactive antifreeze protein from beetles. Nature 388:727–28 [Google Scholar]
  32. Tyshenko MG, Doucet D, Davies PL, Walker VK. 32.  1997. The antifreeze potential of the spruce budworm thermal hysteresis protein. Nat. Biotechnol. 15:887–90 [Google Scholar]
  33. Kawahara H, Iwanaka Y, Higa S, Muryoi N, Sato M. 33.  et al. 2007. A novel, intracellular antifreeze protein in an Antarctic bacterium, Flavobacterium xanthum. CryoLetters 28:39–49 [Google Scholar]
  34. Wharton D, Raymond M. 34.  2015. Cold tolerance of the Antarctic nematodes Plectus murrayi and Scottnema lindsayae. J. Comp. Physiol. B 185:281–89 [Google Scholar]
  35. Griffith M, Yaish MWF. 35.  2004. Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci. 9:399–405 [Google Scholar]
  36. Duman JG. 36.  1994. Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara. Biochim. Biophys. Acta 1206:129–35 [Google Scholar]
  37. Sidebottom C, Buckley S, Pudney P, Twigg S, Jarman C. 37.  et al. 2000. Phytochemistry: heat-stable antifreeze protein from grass. Nature 406:256 [Google Scholar]
  38. Mazur P. 38.  1984. Freezing of living cells: mechanisms and implications. Am. J. Physiol. 247:C125–42 [Google Scholar]
  39. Budke C, Dreyer A, Jaeger J, Gimpel K, Berkemeier T. 39.  et al. 2014. Quantitative efficacy classification of ice recrystallization inhibition agents. Cryst. Growth Des. 14:4285–94 [Google Scholar]
  40. Yu SO, Brown A, Middleton AJ, Tomczak MM, Walker VK, Davies PL. 40.  2010. Ice restructuring inhibition activities in antifreeze proteins with distinct differences in thermal hysteresis. Cryobiology 61:327–34 [Google Scholar]
  41. Worrall D, Elias L, Ashford D, Smallwood M, Sidebottom C. 41.  et al. 1998. A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 282:115–17 [Google Scholar]
  42. Raymond JA, Fritsen C, Shen K. 42.  2007. An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol. Ecol. 61:214–21 [Google Scholar]
  43. Olijve LL, Meiser K, DeVries AL, Duman J, Guo S. 43.  et al. 2016. Blocking rapid ice crystal growth through nonbasal plane adsorption of antifreeze proteins. PNAS 1133740–45
  44. Tomczak MM, Hincha DK, Estrada SD, Feeney RE, Crowe JH. 44.  2001. Antifreeze proteins differentially affect model membranes during freezing. Biochim. Biophys. Acta 1511:255–63 [Google Scholar]
  45. Tomalty HE, Walker VK. 45.  2014. Perturbation of bacterial ice nucleation activity by a grass antifreeze protein. Biochem. Biophys. Res. Commun. 452:636–41 [Google Scholar]
  46. Raymond JA, Janech MG, Fritsen CH. 46.  2009. Novel ice-binding proteins from a psychrophilic Antarctic alga (Chlamydomonadaceae, Chlorophyceae). J. Phycol. 45:130–36 [Google Scholar]
  47. Krembs C, Eicken H, Junge K, Deming JW. 47.  2002. High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep-Sea Res. Part I 49:2163–81 [Google Scholar]
  48. Deming JW. 48.  2002. Psychrophiles and polar regions. Curr. Opin. Microbiol. 5:301–9 [Google Scholar]
  49. Raymond JA, Christner BC, Schuster SC. 49.  2008. A bacterial ice-binding protein from the Vostok ice core. Extremophiles 12:713–17 [Google Scholar]
  50. Janech MG, Krell A, Mock T, Kang JS, Raymond JA. 50.  2006. Ice-binding proteins from sea ice diatoms (Bacillariophyceae). J. Phycol. 42:410–16 [Google Scholar]
  51. Gilbert JA, Davies PL, Laybourn-Parry J. 51.  2005. A hyperactive, Ca2+-dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiol. Lett. 245:67–72 [Google Scholar]
  52. Garnham CP, Gilbert JA, Hartman CP, Campbell RL, Laybourn-Parry J, Davies PL. 52.  2008. A Ca2+-dependent bacterial antifreeze protein domain has a novel β-helical ice-binding fold. Biochem. J. 411:171–80 [Google Scholar]
  53. Guo SQ, Garnham CP, Partha SK, Campbell RL, Allingham JS, Davies PL. 53.  2013. Role of Ca2+ in folding the tandem β-sandwich extender domains of a bacterial ice-binding adhesin. FEBS J. 280:5919–32 [Google Scholar]
  54. Bigg EK. 54.  1953. The supercooling of water. Proc. Phys. Soc. B 66:688 [Google Scholar]
  55. Lindow SE. 55.  1983. The role of bacterial ICE nucleation in frost injury to plants. Annu. Rev. Phytopathol. 21:363–84 [Google Scholar]
  56. Kawahara H, Nakano Y, Omiya K, Muryoi N, Nishikawa J, Obata H. 56.  2004. Production of two types of ice crystal-controlling proteins in Antarctic bacterium. J. Biosci. Bioeng. 98:220–23 [Google Scholar]
  57. Sun X, Griffith M, Pasternak JJ, Glick BR. 57.  1995. Low temperature growth, freezing survival, and production of antifreeze protein by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can. J. Microbiol. 41:776–84 [Google Scholar]
  58. Green RL, Warren GJ. 58.  1985. Physical and functional repetition in a bacterial ice nucleation gene. Nature 317:645–48 [Google Scholar]
  59. Garnham CP, Campbell RL, Walker VK, Davies PL. 59.  2011. Novel dimeric β-helical model of an ice nucleation protein with bridged active sites. BMC Struct. Biol. 11:36 [Google Scholar]
  60. Graether SP, Jia ZC. 60.  2001. Modeling Pseudomonas syringae ice-nucleation protein as a β-helical protein. Biophys. J. 80:1169–73 [Google Scholar]
  61. Wilson PW, Osterday KE, Heneghan AF, Haymet ADJ. 61.  2010. Type I antifreeze proteins enhance ice nucleation above certain concentrations. J. Biol. Chem. 285:34741–45 [Google Scholar]
  62. Kobashigawa Y, Nishimiya Y, Miura K, Ohgiya S, Miura A, Tsuda S. 62.  2005. A part of ice nucleation protein exhibits the ice-binding ability. FEBS Lett. 579:1493–97 [Google Scholar]
  63. Jia ZC, Davies PL. 63.  2002. Antifreeze proteins: an unusual receptor-ligand interaction. Trends Biochem. Sci. 27:101–6 [Google Scholar]
  64. Raymond JA, Kim HJ. 64.  2012. Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLOS ONE 7:e35968 [Google Scholar]
  65. Graham LA, Lougheed SC, Ewart KV, Davies PL. 65.  2008. Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLOS ONE 3:e2616 [Google Scholar]
  66. Sicheri F, Yang DS. 66.  1995. Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature 375:427–31 [Google Scholar]
  67. Sun TJ, Lin FH, Campbell RL, Allingham JS, Davies PL. 67.  2014. An antifreeze protein folds with an interior network of more than 400 semi-clathrate waters. Science 343:795–98 [Google Scholar]
  68. Graham LA, Hobbs RS, Fletcher GL, Davies PL. 68.  2013. Helical antifreeze proteins have independently evolved in fishes on four occasions. PLOS ONE 8:e81285 [Google Scholar]
  69. Knight CA, Cheng CC, DeVries AL. 69.  1991. Adsorption of α-helical antifreeze peptides on specific ice crystal-surface planes. Biophys. J. 59:409–18 [Google Scholar]
  70. Liu Y, Li Z, Lin Q, Kosinski J, Seetharaman J. 70.  et al. 2007. Structure and evolutionary origin of Ca2+-dependent herring type II antifreeze protein. PLOS ONE 2:e548 [Google Scholar]
  71. Nishimiya Y, Kondo H, Takamichi M, Sugimoto H, Suzuki M. 71.  et al. 2008. Crystal structure and mutational analysis of Ca2+-independent type II antifreeze protein from longsnout poacher, Brachyopsis rostratus. J. Mol. Biol. 382:734–46 [Google Scholar]
  72. Jia Z, DeLuca CI, Chao H, Davies PL. 72.  1996. Structural basis for the binding of a globular antifreeze protein to ice. Nature 384:285–88 [Google Scholar]
  73. Hew CL, Wang NC, Joshi S, Fletcher GL, Scott GK. 73.  et al. 1988. Multiple genes provide the basis for antifreeze protein diversity and dosage in the ocean pout, Macrozoarces americanus. J. Biol. Chem. 263:12049–55 [Google Scholar]
  74. Nishimiya Y, Sato R, Takamichi M, Miura A, Tsuda S. 74.  2005. Co-operative effect of the isoforms of type III antifreeze protein expressed in Notched-fin eelpout, Zoarces elongatus Kner. FEBS J. 272:482–92 [Google Scholar]
  75. Baardsnes J, Davies PL. 75.  2001. Sialic acid synthase: the origin of fish type III antifreeze protein?. Trends Biochem. Sci. 26:468–69 [Google Scholar]
  76. Garnham CP, Natarajan A, Middleton AJ, Kuiper MJ, Braslavsky I, Davies PL. 76.  2010. Compound ice-binding site of an antifreeze protein revealed by mutagenesis and fluorescent tagging. Biochemistry 49:9063–71 [Google Scholar]
  77. Liou YC, Tocilj A, Davies PL, Jia ZC. 77.  2000. Mimicry of ice structure by surface hydroxyls and water of a β-helix antifreeze protein. Nature 406:322–24 [Google Scholar]
  78. Duman JG, Li N, Verleye D, Goetz FW, Wu DW. 78.  et al. 1998. Molecular characterization and sequencing of antifreeze proteins from larvae of the beetle Dendroides canadensis. J. Comp. Physiol. B 168:225–32 [Google Scholar]
  79. Qiu L, Wang Y, Wang J, Zhang F, Ma J. 79.  2009. Expression of biologically active recombinant antifreeze protein His-MpAFP149 from the desert beetle (Microdera punctipennis dzungarica) in Escherichia coli. Mol. Biol. Rep. 37:1725–32 [Google Scholar]
  80. Leinala EK, Davies PL, Doucet D, Tyshenko MG, Walker VK, Jia ZC. 80.  2002. A β-helical antifreeze protein isoform with increased activity: structural and functional insights. J. Biol. Chem. 277:33349–52 [Google Scholar]
  81. Graether SP, Kuiper MJ, Gagne SM, Walker VK, Jia ZC. 81.  et al. 2000. β-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature 406:325–28 [Google Scholar]
  82. Hakim A, Nguyen JB, Basu K, Zhu DF, Thakral D. 82.  et al. 2013. Crystal structure of an insect antifreeze protein and its implications for ice binding. J. Biol. Chem. 288:12295–304 [Google Scholar]
  83. Kristiansen E, Wilkens C, Vincents B, Friis D, Lorentzen AB. 83.  et al. 2012. Hyperactive antifreeze proteins from longhorn beetles: some structural insights. J. Insect Physiol. 58:1502–10 [Google Scholar]
  84. Pentelute BL, Gates ZP, Tereshko V, Dashnau JL, Vanderkooi JM. 84.  et al. 2008. X-ray structure of snow flea antifreeze protein determined by racemic crystallization of synthetic protein enantiomers. J. Am. Chem. Soc. 130:9695–701 [Google Scholar]
  85. Graham LA, Davies PL. 85.  2005. Glycine-rich antifreeze proteins from snow fleas. Science 310:461 [Google Scholar]
  86. Mok YF, Lin FH, Graham LA, Celik Y, Braslavsky I, Davies PL. 86.  2010. Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry 49:2593–603 [Google Scholar]
  87. Middleton AJ, Marshall CB, Faucher F, Bar-Dolev M, Braslavsky I. 87.  et al. 2012. Antifreeze protein from freeze-tolerant grass has a β-roll fold with an irregularly structured ice-binding site. J. Mol. Biol. 416:713–24 [Google Scholar]
  88. Kumble KD, Demmer J, Fish S, Hall C, Corrales S. 88.  et al. 2008. Characterization of a family of ice-active proteins from the Ryegrass, Lolium perenne. Cryobiology 57:263–68 [Google Scholar]
  89. Kondo H, Hanada Y, Sugimoto H, Hoshino T, Garnham CP. 89.  et al. 2012. Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation. PNAS 109:9360–65 [Google Scholar]
  90. Garnham CP, Campbell RL, Davies PL. 90.  2011. Anchored clathrate waters bind antifreeze proteins to ice. PNAS 108:7363–67 [Google Scholar]
  91. Vance TDR, Olijve LLC, Campbell RL, Voets IK, Davies PL, Guo SQ. 91.  2014. Ca2+-stabilized adhesin helps an Antarctic bacterium reach out and bind ice. Biosci. Rep. 34:e00121 [Google Scholar]
  92. Koop T, Luo BP, Tsias A, Peter T. 92.  2000. Water activity as the determinant for homogeneous ice nucleation in aqueous solutions. Nature 406:611–14 [Google Scholar]
  93. Bar M, Celik Y, Fass D, Braslavsky I. 93.  2008. Interactions of β-helical antifreeze protein mutants with ice. Cryst. Growth Des. 8:2954–63 [Google Scholar]
  94. Yeh Y, Feeney RE. 94.  1996. Antifreeze proteins: structures and mechanisms of function. Chem. Rev. 96:601–17 [Google Scholar]
  95. Liu ZH, Muldrew K, Wan RG, Elliott JAW. 95.  2003. Measurement of freezing point depression of water in glass capillaries and the associated ice front shape. Phys. Rev. E 67:061602 [Google Scholar]
  96. Wilson PW. 96.  1993. Explaining thermal hysteresis by the Kelvin effect. CryoLetters 14:31–36 [Google Scholar]
  97. Kuiper MJ, Lankin C, Gauthier SY, Walker VK, Davies PL. 97.  2003. Purification of antifreeze proteins by adsorption to ice. Biochem. Biophys. Res. Commun. 300:645–48 [Google Scholar]
  98. Pertaya N, Marshall CB, DiPrinzio CL, Wilen L, Thomson ES. 98.  et al. 2007. Fluorescence microscopy evidence for quasi-permanent attachment of antifreeze proteins to ice surfaces. Biophys. J. 92:3663–73 [Google Scholar]
  99. Kuiper MJ, Morton CJ, Abraham SE, Gray-Weale A. 99.  2015. The biological function of an insect antifreeze protein simulated by molecular dynamics. eLife 4:e05142 [Google Scholar]
  100. Wen DY, Laursen RA. 100.  1992. Structure-function-relationships in an antifreeze polypeptide: the role of neutral, polar amino-acids. J. Biol. Chem. 267:14102–8 [Google Scholar]
  101. Scotter AJ, Marshall CB, Graham LA, Gilbert JA, Garnham CP, Davies PL. 101.  2006. The basis for hyperactivity of antifreeze proteins. Cryobiology 53:229–39 [Google Scholar]
  102. Can O, Holland NB. 102.  2009. Modified Langmuir isotherm for a two-domain adsorbate: derivation and application to antifreeze proteins. J. Colloid Interface Sci. 329:24–30 [Google Scholar]
  103. Liu JJ, Li QZ. 103.  2006. Theoretical model of antifreeze protein-ice adsorption: binding of large ligands to a two-dimensional homogeneous lattice. Chem. Phys. Lett. 422:67–71 [Google Scholar]
  104. Takamichi M, Nishimiya Y, Miura A, Tsuda S. 104.  2007. Effect of annealing time of an ice crystal on the activity of type III antifreeze protein. FEBS J. 274:6469–76 [Google Scholar]
  105. Drori R, Celik Y, Davies PL, Braslavsky I. 105.  2014. Ice-binding proteins that accumulate on different ice crystal planes produce distinct thermal hysteresis dynamics. J. R. Soc. Interface 11:20140526 [Google Scholar]
  106. Kristiansen E, Zachariassen KE. 106.  2005. The mechanism by which fish antifreeze proteins cause thermal hysteresis. Cryobiology 51:262–80 [Google Scholar]
  107. Pertaya N, Marshall CB, Celik Y, Davies PL, Braslavsky I. 107.  2008. Direct visualization of spruce budworm antifreeze protein interacting with ice crystals: Basal plane affinity confers hyperactivity. Biophys. J. 95:333–41 [Google Scholar]
  108. Drori R, Davies PL, Braslavsky I. 108.  2015. Experimental correlation between thermal hysteresis activity and the distance between antifreeze proteins on an ice surface. RSC Adv. 5:7848–53 [Google Scholar]
  109. Nutt DR, Smith JC. 109.  2008. Function of the hydration layer around an antifreeze protein revealed by atomistic molecular dynamics simulations. J. Am. Chem. Soc. 130:13066–73 [Google Scholar]
  110. Sharp KA. 110.  2014. The remarkable hydration of the antifreeze protein Maxi: a computational study. J. Chem. Phys. 141:22D510 [Google Scholar]
  111. Ohno H, Susilo R, Gordienko R, Ripmeester J, Walker VK. 111.  2010. Interaction of antifreeze proteins with hydrocarbon hydrates. Chem. Eur. J. 16:10409–17 [Google Scholar]
  112. Bagherzadeh SA, Alavi S, Ripmeestera JA, Englezos P. 112.  2015. Why ice-binding type I antifreeze protein acts as a gas hydrate crystal inhibitor. Phys. Chem. Chem. Phys. 17:9984–90 [Google Scholar]
  113. Sun T, Davies PL, Walker VK. 113.  2015. Structural basis for the inhibition of gas hydrates by α-helical antifreeze proteins. Biophys. J. 109:1698–705 [Google Scholar]
  114. Meister K, Strazdaite S, DeVries AL, Lotze S, Olijve LLC. 114.  et al. 2014. Observation of ice-like water layers at an aqueous protein surface. PNAS 111:17732–36 [Google Scholar]
  115. Meister K, Lotze S, Olijve LLC, DeVries AL, Duman JG. 115.  et al. 2015. Investigation of the ice-binding site of an insect antifreeze protein using sum-frequency generation spectroscopy. J. Phys. Chem. Lett. 6:1162–67 [Google Scholar]
  116. Ebbinghaus S, Meister K, Born B, DeVries AL, Gruebele M, Havenith M. 116.  2010. Antifreeze glycoprotein activity correlates with long-range protein–water dynamics. J. Am. Chem. Soc. 132:12210–11 [Google Scholar]
  117. Ebbinghaus S, Meister K, Prigozhin MB, DeVries AL, Havenith M. 117.  et al. 2012. Functional importance of short-range binding and long-range solvent interactions in helical antifreeze peptides. Biophys. J. 103:L20–22 [Google Scholar]
  118. Meister K, Ebbinghaus S, Xu Y, Duman JG, DeVries A. 118.  et al. 2013. Long-range protein–water dynamics in hyperactive insect antifreeze proteins. PNAS 110:1617–22 [Google Scholar]
  119. De Yoreo JJ, Dove PM. 119.  2004. Shaping crystals with biomolecules. Science 306:1301–2 [Google Scholar]
  120. Addadi L, Weiner S. 120.  1985. Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. PNAS 82:4110–14 [Google Scholar]
  121. Antson AA, Smith DJ, Roper DI, Lewis S, Caves LSD. 121.  et al. 2001. Understanding the mechanism of ice binding by type III antifreeze proteins. J. Mol. Biol. 305:875–89 [Google Scholar]
  122. Basu K, Garnham CP, Nishimiya Y, Tsuda S, Braslavsky I, Davies P. 122.  2014. Determining the ice-binding planes of antifreeze proteins by fluorescence-based ice plane affinity. J Vis. Exp. 83:e51185 [Google Scholar]
  123. Sørensen TF, Ramløv H. 123.  2001. Variations in antifreeze activity and serum inorganic ions in the eelpout Zoarces viviparus: antifreeze activity in the embryonic state. Comp. Biochem. Physiol. A 130:123–32 [Google Scholar]
  124. Li N, Andorfer CA, Duman JG. 124.  1998. Enhancement of insect antifreeze protein activity by solutes of low molecular mass. J. Exp. Biol. 201:2243–51 [Google Scholar]
  125. Evans RP, Hobbs RS, Goddard SV, Fletcher GL. 125.  2007. The importance of dissolved salts to the in vivo efficacy of antifreeze proteins. Comp. Biochem. Physiol. A 148:556–61 [Google Scholar]
  126. Wu DW, Duman JG, Xu L. 126.  1991. Enhancement of insect antifreeze protein activity by antibodies. Biochim. Biophys. Acta 1076:416–20 [Google Scholar]
  127. Lin X, Wisniewski M, Duman JG. 127.  2011. Expression of two self-enhancing antifreeze proteins from the beetle Dendroides canadensis in Arabidopsis thaliana. Plant Mol. Biol. Rep. 29:802–13 [Google Scholar]
  128. Wang L, Duman JG. 128.  2006. A thaumatin-like protein from larvae of the beetle Dendroides canadensis enhances the activity of antifreeze proteins. Biochemistry 45:1278–84 [Google Scholar]
  129. Yang SH, Wojnar JM, Harris PWR, DeVries AL, Evans CW, Brimble MA. 129.  2013. Chemical synthesis of a masked analogue of the fish antifreeze potentiating protein (AFPP). Org. Biomol. Chem. 11:4935–42 [Google Scholar]
  130. DeVries AL. 130.  1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172:1152–55 [Google Scholar]
  131. Chao H, Hodges RS, Kay CM, Gauthier SY, Davies PL. 131.  1996. A natural variant of type I antifreeze protein with four ice-binding repeats is a particularly potent antifreeze. Protein Sci. 5:1150–56 [Google Scholar]
  132. DeLuca CI, Comley R, Davies PL. 132.  1998. Antifreeze proteins bind independently to ice. Biophys. J. 74:1502–8 [Google Scholar]
  133. Baardsnes J, Kuiper MJ, Davies PL. 133.  2003. Antifreeze protein dimer: when two ice-binding faces are better than one. J. Biol. Chem. 278:38942–47 [Google Scholar]
  134. Marshall CB, Daley ME, Sykes BD, Davies PL. 134.  2004. Enhancing the activity of a β-helical antifreeze protein by the engineered addition of coils. Biochemistry 43:11637–46 [Google Scholar]
  135. Wang X, DeVries AL, Cheng CHC. 135.  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 1247:163–72 [Google Scholar]
  136. DeVries AL, Vandenheede J, Feeney RE. 136.  1971. Primary structure of freezing point-depressing glycoproteins. J. Biol. Chem. 246:305–8 [Google Scholar]
  137. Marshall CB, Fletcher GL, Davies PL. 137.  2004. Hyperactive antifreeze protein in a fish. Nature 429:153–53 [Google Scholar]
  138. Peralta MDR, Karsai A, Ngo A, Sierra C, Fong KT. 138.  et al. 2015. Engineering amyloid fibrils from β-solenoid proteins for biomaterials applications. ACS Nano 9:1449–63 [Google Scholar]
  139. Knight CA, Wen D, Laursen RA. 139.  1995. Nonequilibrium antifreeze peptides and the recrystallization of ice. Cryobiology 32:23–34 [Google Scholar]
  140. Budke C, Koop T. 140.  2006. Ice recrystallization inhibition and molecular recognition of ice faces by poly(vinyl alcohol). ChemPhysChem 7:2601–6 [Google Scholar]
  141. Inada T, Lu SS. 141.  2003. Inhibition of recrystallization of ice grains by adsorption of poly(vinyl alcohol) onto ice surfaces. Cryst. Growth Des. 3:747–52 [Google Scholar]
  142. Deville S, Viazzi C, Leloup J, Lasalle A, Guizard C. 142.  et al. 2011. Ice shaping properties, similar to that of antifreeze proteins, of a zirconium acetate complex. PLOS ONE 6:e26474 [Google Scholar]
  143. Mizrahy O, Bar-Dolev M, Guy S, Braslavsky I. 143.  2013. Inhibition of ice growth and recrystallization by zirconium acetate and zirconium acetate hydroxide. PLOS ONE 8:e59540 [Google Scholar]
  144. Gibson MI. 144.  2010. Slowing the growth of ice with synthetic macromolecules: beyond antifreeze (glyco)proteins. Polym. Chem. 1:1141–52 [Google Scholar]
  145. Hachisu M, Hinou H, Takamichi M, Tsuda S, Koshidaa S, Nishimura SI. 145.  2009. One-pot synthesis of cyclic antifreeze glycopeptides. Chem. Commun. 13:1641–43 [Google Scholar]
  146. Ahn M, Murugan RN, Shin SY, Kim E, Lee JH. 146.  et al. 2012. Synthesis of cyclic antifreeze glycopeptide and glycopeptoids and their ice recrystallization inhibition activity. Bull. Korean Chem. Soc. 33:3565–70 [Google Scholar]
  147. Wierzbicki A, Knight CA, Rutland TJ, Muccio DD, Pybus BS, Sikes CS. 147.  2000. Structure–function relationship in the antifreeze activity of synthetic alanine–lysine antifreeze polypeptides. Biomacromolecules 1:268–74 [Google Scholar]
  148. Walters KR, Serianni AS, Sformo T, Barnes BM, Duman JG. 148.  2009. A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. PNAS 106:20210–15 [Google Scholar]
  149. Walters K Jr., Serianni A, Voituron Y, Sformo T, Barnes B, Duman J. 149.  2011. A thermal hysteresis-producing xylomannan glycolipid antifreeze associated with cold tolerance is found in diverse taxa. J. Comp. Physiol. B 181:631–40 [Google Scholar]
  150. Crich D, Rahaman MY. 150.  2011. Synthesis and structural verification of the xylomannan antifreeze substance from the freeze-tolerant Alaskan beetle Upis ceramboides. J. Org. Chem. 76:8611–20 [Google Scholar]
  151. Brockbank KGM, Campbell LH, Greene ED, Brockbank MCG, Duman JG. 151.  2011. Lessons from nature for preservation of mammalian cells, tissues, and organs. In Vitro Cell. Dev. Biol. 47:210–17 [Google Scholar]
  152. Bang JK, Lee JH, Murugan RN, Lee SG, Do H. 152.  et al. 2013. Antifreeze peptides and glycopeptides, and their derivatives: potential uses in biotechnology. Mar. Drugs 11:2013–41 [Google Scholar]
  153. Arav A, Rubinsky B, Fletcher G, Seren E. 153.  1993. Cryogenic protection of oocytes with antifreeze proteins. Mol. Reprod. Dev. 36:488–93 [Google Scholar]
  154. Ideta A, Aoyagi Y, Tsuchiya K, Nakamura Y, Hayama K. 154.  et al. 2015. Prolonging hypothermic storage (4 C) of bovine embryos with fish antifreeze protein. J. Reprod. Dev. 61:1–6 [Google Scholar]
  155. Kamijima T, Sakashita M, Miura A, Nishimiya Y, Tsuda S. 155.  2013. Antifreeze protein prolongs the life-time of insulinoma cells during hypothermic preservation. PLOS ONE 8:e73643 [Google Scholar]
  156. Rubinsky L, Raichman N, Lavee J, Frenk H, Ben-Jacob E, Bickler PE. 156.  2010. Antifreeze protein suppresses spontaneous neural activity and protects neurons from hypothermia/re-warming injury. Neurosci. Res. 67:256–59 [Google Scholar]
  157. Hirano Y, Nishimiya Y, Matsumoto S, Matsushita M, Todo S. 157.  et al. 2008. Hypothermic preservation effect on mammalian cells of type III antifreeze proteins from notched-fin eelpout. Cryobiology 57:46–51 [Google Scholar]
  158. Amir G, Rubinsky B, Basheer SY, Horowitz L, Jonathan L. 158.  et al. 2005. Improved viability and reduced apoptosis in sub-zero 21-hour preservation of transplanted rat hearts using anti-freeze proteins. J. Heart Lung Transplant. 24:1915–29 [Google Scholar]
  159. Amir G, Rubinsky B, Horowitz L, Miller L, Leor J. 159.  et al. 2004. Prolonged 24-hour subzero preservation of heterotopically transplanted rat hearts using antifreeze proteins derived from arctic fish. Ann. Thorac. Surg. 77:1648–55 [Google Scholar]
  160. Heisig M, Mattessich S, Rembisz A, Acar A, Shapiro M. 160.  et al. 2015. Frostbite protection in mice expressing an antifreeze glycoprotein. PLOS ONE 10:e0116562 [Google Scholar]
  161. Jo JW, Jee BC, Lee JR, Suh CS. 161.  2011. Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence. Fertil. Steril. 96:1239–45 [Google Scholar]
  162. Qadeer S, Khan MA, Ansari MS, Rakha BA, Ejaz R. 162.  et al. 2015. Efficiency of antifreeze glycoproteins for cryopreservation of Nili-Ravi (Bubalus bubalis) buffalo bull sperm. Anim. Reprod. Sci. 157:56–62 [Google Scholar]
  163. Zilli L, Beirao J, Schiavone R, Herraez MP, Gnoni A, Vilella S. 163.  2014. Comparative proteome analysis of cryopreserved flagella and head plasma membrane proteins from sea bream spermatozoa: effect of antifreeze proteins. PLOS ONE 9:e99992 [Google Scholar]
  164. Nishijima K, Tanaka M, Sakai Y, Koshimoto C, Morimoto M. 164.  et al. 2014. Effects of type III antifreeze protein on sperm and embryo cryopreservation in rabbit. Cryobiology 69:22–25 [Google Scholar]
  165. Ishiguro H, Rubinsky B. 165.  1998. Influence of fish antifreeze proteins on the freezing of cell suspensions with cryoprotectant penetrating cells. Int. J. Heat Mass Transf. 41:1907–15 [Google Scholar]
  166. Rubinsky B, DeVries AL. 166.  1989. Effect of ice crystal habit on the viability of glycerol-protected red blood cells. Cryobiology 26:580 [Google Scholar]
  167. Koushafar H, Rubinsky B. 167.  1997. Effect of antifreeze proteins on frozen primary prostatic adenocarcinoma cells. Urology 49:421–25 [Google Scholar]
  168. Halwani DO, Brockbank KGM, Duman JG, Campbell LH. 168.  2014. Recombinant Dendroides canadensis antifreeze proteins as potential ingredients in cryopreservation solutions. Cryobiology 68:411–18 [Google Scholar]
  169. Rubinsky B. 169.  2000. Cryosurgery. Annu. Rev. Biomed. Eng. 2:157–87 [Google Scholar]
  170. Baust JG, Bischof JC, Jiang-Hughes S, Polascik TJ, Rukstalis DB. 170.  et al. 2015. Re-purposing cryoablation: a combinatorial “therapy” for the destruction of tissue. Prostate Cancer Prostatic Dis. 18:87–95 [Google Scholar]
  171. Cook KLK, Hartel RW. 171.  2010. Mechanisms of ice crystallization in ice cream production. Compr. Rev. Food Sci. Food Saf. 9:213–22 [Google Scholar]
  172. Payne SR, Sandford D, Harris A, Young OA. 172.  1994. The effects of antifreeze proteins on chilled and frozen meat. Meat Sci. 37:429–38 [Google Scholar]
  173. Zhang R, Zhang J, Wei J, Liu C, Yang J. 173.  et al. 2015. Deep research report on global antifreeze proteins (AFP) industry81–82 QYResearch Antifreeze Proteins Research Center, Haidian District, Beijing, China
  174. Breton G, Danyluk J, Ouellet F, Sarhan F. 174.  2000. Biotechnological applications of plant freezing associated proteins. Biotechnology Annual Review MR El-Gewely 59–101 New York: Elsevier Sci. [Google Scholar]
  175. Khanna HK, Daggard GE. 175.  2006. Targeted expression of redesigned and codon optimised synthetic gene leads to recrystallisation inhibition and reduced electrolyte leakage in spring wheat at sub-zero temperatures. Plant Cell Rep. 25:1336–46 [Google Scholar]
  176. Hightower R, Baden C, Penzes E, Lund P, Dunsmuir P. 176.  1991. Expression of antifreeze proteins in transgenic plants. Plant Mol. Biol. 17:1013–21 [Google Scholar]
  177. Kenward KD, Brandle J, McPherson J, Davies PL. 177.  1999. Type II fish antifreeze protein accumulation in transgenic tobacco does not confer frost resistance. Transgenic Res. 8:105–17 [Google Scholar]
  178. Zhu B, Xiong A-S, Peng R-H, Xu J, Jin X-F. 178.  et al. 2010. Over-expression of ThpI from Choristoneura fumiferana enhances tolerance to cold in Arabidopsis. Mol. Biol. Rep. 37:961–66 [Google Scholar]
  179. Fletcher GL, Shears MA, Yaskowiak ES, King MJ, Goddard SV. 179.  2004. Gene transfer: potential to enhance the genome of Atlantic salmon for aquaculture. Aust. J. Exp. Agric. 44:1095–2100 [Google Scholar]
  180. Nicodemus J, O'Tousa JE, Duman JG. 180.  2006. Expression of a beetle, Dendroides canadensis, antifreeze protein in Drosophila melanogaster. J. Insect Physiol. 52:888–96 [Google Scholar]
  181. Wang R, Zhang P, Gong Z, Hew CL. 181.  1995. Expression of the antifreeze protein gene in transgenic goldfish (Carassius auratus) and its implication in cold adaptation. Mol. Mar. Biol. Biotechnol. 4:20–26 [Google Scholar]
  182. Van Eenennaam AL, Muir WM. 182.  2011. Transgenic salmon: a final leap to the grocery shelf?. Nat. Biotechnol. 29:706–10 [Google Scholar]
  183. Lv J, Song Y, Jiang L, Wang J. 183.  2014. Bio-inspired strategies for anti-icing. ACS Nano 8:3152–69 [Google Scholar]
  184. Rykaczewski K, Anand S, Subramanyam SB, Varanasi KK. 184.  2013. Mechanism of frost formation on lubricant-impregnated surfaces. Langmuir 29:5230–38 [Google Scholar]
  185. Esser-Kahn AP, Trang V, Francis MB. 185.  2010. Incorporation of antifreeze proteins into polymer coatings using site-selective bioconjugation. J. Am. Chem. Soc. 132:13264–69 [Google Scholar]
  186. Gwak Y, Park J-i, Kim M, Kim HS, Kwon MJ. 186.  et al. 2015. Creating anti-icing surfaces via the direct immobilization of antifreeze proteins on aluminum. Sci. Rep. 5:12019 [Google Scholar]
  187. Lewis JK, Bischof JC, Braslavsky I, Brockbanke KGM, Fahy GM. 187.  et al. 2015. The grand challenges of organ banking: proceedings from the first global summit on complex tissue cryopreservation. Cryobiology 72169–82
/content/journals/10.1146/annurev-biochem-060815-014546
Loading
Ice-Binding Proteins and Their Function
Annual Review of Biochemistry 85, 515 (2016); https://doi.org/10.1146/annurev-biochem-060815-014546
/content/journals/10.1146/annurev-biochem-060815-014546
/content/journals/10.1146/annurev-biochem-060815-014546
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error