ОСНОВНЫЕ СВОЙСТВА И ОСОБЕННОСТИ ЭВОЛЮЦИИ АНТИФРИЗНЫХ БЕЛКОВ

Антифризные белки представляют собой класс белков, синтезируемых пойкилотермными организмами при холодовом стрессе. Эти белки имеют разное эволюционное происхождение, отличаются по первичной и вторичной структуре, механизму регуляции, однако все они имеют общее качество – способность адсорбироваться на поверхность кристаллов льда и модифицировать их рост. В обзоре c акцентом на злаковые растения, в том числе пшеницу, обобщены данные о происхождении антифризных белков, их таксономическом распространении, свойствах и особенностях функционирования.

1. Самыгин Г.А. Образование льда в растениях // Физиол. растений. 1997. Т. 44. № 2. С. 275–286.

2. Трунова Т.И. Растение и низкотемпературный стресс. М.: Наука, 2007. 54 с.

3. Amornwittawat N., Wang S., Duman J.G. et al. Polycarboxylates enhance beetle antifreeze protein activity // Biochim. Biophys. Acta. 2008. V. 1784. Nо 12. P. 1942–1948.

4. Andorfer C.A., Duman J.G. Isolation and characterization of cDNA clones encoding antifreeze proteins of the pyrochroid beetle Dendroides canadensis // J. Insect Physiol. 2000. V. 46. P. 365–372.

5. Antikainen M., Griffith M. Antifreeze accumulation in freezing tolerant cereals // Physiol. Plant. 1997. V. 99. P. 423–432.

6. Antikainen M., Griffi th M., Zhang J. et al. Immunolocalization of antifreeze proteins in winter rye leaves, crowns, and roots by tissue printing // Plant Physiol. 1996. V. 110. P. 845–857.

7. Baardsnes J., Kondejewski L.H., Hodges R.S. et al. New icebinding face for type I antifreeze protein // FEBS Lett. 1999. V. 463. Nо 1/2. P. 87–91.

8. Baardsnes J., Kuiper M.J., Davies P.L. Antifreeze protein dimer: when two ice-binding faces are better than one // J. Biol. Chem. 2003. V. 278. Nо 40. P. 38942–38947.

9. Barrett J. Thermal hysteresis proteins // Int. J. Biochem. Cell Biol. 2001. V. 33. Nо 2. P. 105–117.

10. Bayer-Giraldi M., Weikusat I., Besir H. et al. Characterization of an antifreeze protein from the polar diatom Fragilariopsis cylindrus and its relevance in sea ice // Cryobiology. 2011. V. 63. Nо 3. P. 210–219.

11. Bilyk K.T., DeVries A.L. Delayed onset of adult antifreeze activity juveniles of the Antarctic icefi sh Chaenocephalus aceratus // Polar Biol. 2011. DOI 10.1007/s00300-010- 0828-6 (Published on line).

12. Bouvet V.R., Lorello G.R., Ben R.N. Aggregation of antifreeze glycoprotein fraction 8 and its effect on antifreeze activity // Biomacromol. 2006. V. 7. Nо 2. P. 565–571.

13. Bravo L.A., Griffith M. Characterization of antifreeze activity in Antarctic plants // J. Exp. Bot. 2005. V. 56. P. 1189–1196.

14. Cheng C.H. Origin and mechanism of evolution of antifreeze glycoproteins in polar fi shes // Evolution of the Antarctic Ichthyofauna / Eds G. di Prisco, E. Pisano, A. Clarke. Springer-Verlag, Italy, 1998. P. 311–328.

15. Cheng C.H., Chen L. Evolution of an antifreeze glycoprotein// Nature. 1999. V. 401. Nо 6752. P. 443–444.

16. Cziko P.A., Evans C.W., Cheng C.-H.C. et al. Freezing resistance of antifreeze-defi cient larval Antarctic fi sh // J. Exp. Biol. 2006. V. 209. P. 407–420.

17. Davies P.L., Baardsnes J., Kuiper M.J. et al. Structure and function of antifreeze proteins // Phil. Trans. R. Soc. Lond. B. 2002. V. 357. P. 927–935.

18. Davies P.L., Sykes B.D. Antifreeze proteins // Curr. Opin. Struct. Biol. 1997. V. 7. P. 828–834.

19. Deng C., Cheng C.H., Ye H. et al. Evolution of an antifreeze protein by neofunctionalization under escape from adaptive confl ict // Proc. Natl Acad. Sci. USA. 2010. V. 107. Nо 50. P. 21593–21598.

20. Desjardins M., Le Franзois N.R., Fletcher G.L. et al. Seasonal modulation of plasma antifreeze protein levels in Atlantic (Anarhichas lupus) and spotted wolffi sh (A. minor) // J. Exp. Mar. Biol. Ecol. 2006. V. 335. P. 142–150.

21. DeVries A.L. Antifreeze glycopeptides and peptides: interactions with ice and water // Methods in Enzymology. 1986. V. 127. P. 293–303.

22. DeVries A.L., Wohlschlag D.E. Freezing resistance in some Antarctic fi shes // Sci. 1969. V. 163. P. 1073–1075.

23. Doucet C.J., Byass L., Elias L. et al. Distribution and characterization of recrystallization inhibitor activity in plant and lichen species from the UK and maritime Antarctic // Cryobiology. 2000. V. 40. Nо 3. P. 218–227.

24. Doucet D., Walker V.K., Qin W. The bugs that came in from the cold: molecular adaptations to low temperatures in insects // Cell Mol. Life Sci. 2009. V. 66. Nо 8. P. 1404–1418.

25. Duman J.G. Purifi cation and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara // Biochim. Biophys. Acta. 1994. V. 1206. P. 129–135.

26. Duman J.G., Bennett V., Sformo T. et al. Antifreeze proteins in Alaskan insects and spiders // J. Insect Physiol. 2004. V. 50. P. 259–266.

27. Duman J.G., Olsen T.M. Thermal hysteresis protein activity in bacteria, fungi and phylogenetically diverse plants // Cryobiology. 1993. V. 30. P. 322–328.

28. Duman J.G., Verleye D., Li N. Site-specifi c forms of antifreeze protein in the beetle Dendroides canadensis // J. Comp. Physiol. [B]. 2002. V. 172. Nо 6. P. 547–552.

29. Duncker B.P., Koops M.D., Walker V.K. et al. Low temperature persistence of type I antifreeze protein is mediated by cold-specifi c mRNA stability // FEBS Lett. 1995. V. 377. P. 185–188.

30. Ebbinghaus S., Meister K., Born B. et al. Antifreeze glycoprotein activity correlates with long-range protein-water dynamics // J. Am. Chem. Soc. 2010. V. 132. Nо 35. P. 12210–12211.

31. Evans R.P., Fletcher G.L. Type I antifreeze proteins: possible origins from chorion and keratin genes in Atlantic snailfi sh // J. Mol. Evol. 2005. V. 61. Nо 4. P. 417–424.

32. Evans R.P., Hobbs R.S., Goddard S.V. et al. The importance of dissolved salts to the in vivo effi cacy of antifreeze proteins // Comp. Biochem. Physiol. Mol. Integr. Physiol. 2007. V. 148. Nо 3. P. 556–561.

33. Ewart K.V., Li Z., Yang D.S. et al. The ice-binding site of Atlantic herring antifreeze protein corresponds to the carbohydrate-binding site of C-type lectins // Biochemistry. 1998. V. 37. Nо 12. P. 4080–4085.

34. Ewart K.V., Lin Q. Hew C.L. Structure, function and evolution of antifreeze proteins // Cell. Mol. Life Sci. 1999. V. 55. P. 271–283.

35. Fei Y.B., Cao P.X., Gao S.Q. et al. Purifi cation and structure analysis of antifreeze proteins from Ammopiptanthus mongolicus // Prep. Biochem. Biotechnol. 2008. V. 38. Nо 2. P. 172–183.

36. Fletcher G.L., Goddard S.V., Wu Y. Antifreeze proteins and their genes: from basic research to business opportunity // Chemtech. 1999. V. 30. P. 17–28.

37. Fletcher G.L., Hew C.L., Davies P.L. Antifreeze proteins of teleost fishes // Annu. Rev. Physiol. 2001. V. 63. P. 359–390.

38. Garnham C.P., Campbell R.L., Davies P.L. Anchored clathrate waters bind antifreeze proteins to ice // Proc. Natl Acad. Sci. USA. 2011. V. 108. Nо 18. P. 7363–7367.

39. Gauthier S.Y., Marshall C.B., Fletcher G.L. et al. Hyperactive antifreeze protein in fl ounder species. The sole freeze protectant in American plaice // FEBS J. 2005. V. 272. Nо 17. P. 4439–4449.

40. Gilbert J.A., Davies P.L., Laybourn-Parry J. A hyperactive, Ca2+–dependent antifreeze protein in an Antarctic bacterium // JFEMS Microbiol. Lett. 2005. V. 245. Nо 1. P. 67–72.

41. Gong Z., Ewart K.V., Hu Z. et al. Skin antifreeze protein genes of the winter fl ounder, Pleuronectes americanus, encode distinct and active polypeptides without the secretory signal and prosequences // J. Biol. Chem. 1996. V. 271. P. 4106–4112.

42. Gong Z., King M.J., Fletcher G.L. et al. The antifreeze protein genes of the winter fl ounder, Pleuronectes americanus, are differentially regulated in liver and non-liver tissues // Biochem. Biophys. Res. Commun. 1995. V. 206. P. 387–392.

43. Gozzo F. Systemic acquired resistance in crop protection: from nature to a chemical approach // J. Agric. Food Chem. 2003. V. 51. Nо 16. P. 4487–4503.

44. Graether S.P., Kuiper M.J., Gagne S.M. et al. Beta-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect // Nature. 2000. V. 406. Nо 6793. P. 249–251.

45. Graether S.P., Sykes B.D. Cold survival in freeze-intolerant insects: the structure and function of beta-helical antifreeze proteins // Eur. J. Biochem. 2004. V. 271. Nо 16. P. 3285–3296.

46. Graham L.A., Davies P.L. Glycine-rich antifreeze proteins from snow fl eas // Sci. 2005. V. 310. P. 461.

47. Graham L.A., Liou Y.C., Walker V.K. et al. Hyperactive antifreeze protein from beetles // Nature. 1997. V. 388. Nо 6644. P. 727–728.

48. Graham L.A., Lougheed S.C., Ewart K.V. et al. Lateral transfer of a lectin-like antifreeze protein gene in fi shes // PLoS ONE. 2008a. V. 3. Nо 7. P. e2616.

49. Graham L.A., Marshall C.B., Lin F.H. et al. Hyperactive antifreeze protein from fi sh contains multiple ice-binding sites // Biochemistry. 2008b. V. 47. Nо 7. P. 2051–2063.

50. Graham L.A., Qin W., Lougheed S.C. et al. Evolution of hyperactive, repetitive antifreeze proteins in beetles // J. Mol. Evol. 2007. V. 64. Nо 4. P. 387–398.

51. Graham L.A., Walker V.K., Davies P.L. Developmental and environmental regulation of antifreeze proteins in the mealworm beetle Tenebrio molitor // Eur. J. Biochem. 2000. V. 267. P. 6452–6458.

52. Griffi th M., Yaish M.W. Antifreeze proteins in overwintering plants: a tale of two activities // Trends Plant. Sci. 2004. V. 9. Nо 8. P. 399–405.

53. Hawes T.C., Marshall C.J., Wharton D.A. Antifreeze proteins in the Antarctic springtail, Gressittacantha terranova // J. Comp. Physiol. B. 2011. V. 181. Nо 6. P. 713–719.

54. Harding M.M., Anderberg P.I., Haymet A.D. ‘Antifreeze’ glycoproteins from polar fi sh // Eur. J. Biochem. 2003. V. 270. Nо 7. P. 1381–1392.

55. Harding M.M., Ward L.G., Haymet A.D. Type I ‘antifreeze’ proteins. Structure–activity studies and mechanisms of ice growth inhibition // Eur. J. Biochem. 1999. V. 264. Nо 3. P. 653–665.

56. Hew C. L., Wang N. C., Joshi S. et al. Multiple genes provide the basis for antifreeze protein diversity and dosage in the ocean pout, Macrozoarces americanus // J. Biol. Chem. 1988. V. 263. P. 12049–12055.

57. Hobbs R.S., Shears M.A., Graham L.A. et al. Isolation and characterization of type I antifreeze proteins from cunner, Tautogolabrus adspersus, order Perciformes // FEBS J. 2011 V. 278. Nо 19. P. 3699–3710.

58. Hon W.C., Griffi th M., Mlynarz A. et al. Antifreeze proteins in winter rye are similar to pathogenesis-related proteins // Plant Physiol. 1995. V. 109. P. 879–889.

59. Horwath K.L., Duman J.G. Induction of antifreeze protein production by juvenile hormone in larvae of the beetle, Dendroides canadensis // J. Comp. Physiol. 1983. V. 151. P. 233–240.

60. Hsiao K.C., Cheng C.H., Fernandes I.E. et al. An antifreeze glycopeptide gene from the antarctic cod Notothenia coriiceps neglecta encodes a polyprotein of high peptide copy number // Proc. Natl Acad. Sci. USA. 1990. V. 87. Nо 23. P. 9265–9269.

61. Huang T., Duman J.G. Cloning and characterization of a thermal hysteresis (antifreeze) protein with DNA-binding activity from winter bittersweet nightshade, Solanum dulcamara // Plant. Mol. Biol. 2002. V. 48. Nо 4. P. 339–350.

62. Janech M.G., Krell A., Mock T. et al. Ice-binding proteins from sea ice diatoms (Bacillariophyceae) // J. Phycol. 2006. V. 42. Nо 2. P. 410–416.

63. Jarzabek M., Pukacki P.M., Nuc K. Cold-regulated proteins with potent antifreeze and cryoprotective activities in spruces (Picea sp.) // Cryobiology. 2009. V. 58. P. 268–274.

64. Jia Z., Davies P.L. Antifreeze proteins: an unusual receptor ligand interaction // Trends Biochem. Sci. 2002. V. 27. Nо 2. P. 101–106.

65. Jin Y., DeVries A.L. Antifreeze glycoprotein levels in Antarctic notothenioid fi shes inhabiting different thermal environments and the effect of warm acclimation // Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 2006. V. 144. Nо 3. P. 290–300.

66. John U.P., Polotnianka R.M., Sivakumaran K.A. et al. Ice recrystallization inhibition proteins (IRIPs) and freeze tolerance in the cryophilic Antarctic hair grass Deschampsia antarctica E. Desv // Plant, Cell and Environment. 2009. V. 32. Nо 4. P. 336–348.

67. Knight C.A., Cheng C.C., DeVries A.L. Adsorption of alphahelical antifreeze peptides on specifi c ice crystal surface planes // Biophys J. 1991. V. 59. Nо 2. P. 409–418.

68. Knight C.A., DeVries A.L. 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. 2009. V. 11. Nо 27. P. 5749–5761.

69. Knight C.A., DeVries A.L., Oolman L.D. Fish antifreeze protein and the freezing and recrystallization of ice // Nature. 1984. V. 308. P. 295–296.

70. Knight C.A., Wen D., Laursen R.A. Nonequilibrium antifreeze peptides and the recrystallization of ice // Cryobiology. 1995. V. 32. P. 23–34.

71. Kristiansen E., Pedersen S.A., Zachariassen K.E. Salt-induced enhancement of antifreeze protein activity: a salting-out effect // Cryobiology. 2008. V. 57. Nо 2. P. 122–129.

72. Kristiansen E., Ramlшv H., Hagen L. et al. Isolation and characterization of hemolymph antifreeze proteins from larvae of the longhorn beetle Rhagium inquisitor (L.) // Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 2005. V. 142. Nо 1. P. 90–97.

73. Kristiansen E., Ramlшv H., Hшjrup P. et al. Structural characteristics of a novel antifreeze protein from the longhorn beetle Rhagium inquisitor // Insect Biochem. Mol. Biol. 2011. V. 41. Nо 2. P. 109–117.

74. Kristiansen E., Pedersen S.A., Ramlшv H. et al. Antifreeze activity in the cerambycid beetle Rhagium inquisitor // J. Comp. Physiol. B. 1999. V. 169. P. 55–60.

75. Kristiansen E., Zachariassen K.E. The mechanism by which fish antifreeze proteins cause thermal hysteresis // Cryobiology. 2005. V. 51. Nо 3. P. 262–280.

76. Laursen K.J., Brown A.J., Middleton A.J. et al. Expression and characterization of an antifreeze protein from the perennial rye grass, Lolium perenne // Cryobiology. 2011. V. 62. P. 194–201.

77. Lee J.K., Park K.S., Park S. et al. An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast // Cryobiology. 2010. V. 60. Nо 2. P. 222–228.

78. Lee J.K., Kim Y.J., Park K.S. et al. Molecular and comparative analyses of type IV antifreeze proteins (AFPIVs) from two Antarctic fi shes, Pleuragramma antarcticum and Notothenia coriiceps // Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2011. V. 159. Nо 4. P. 197–205.

79. Leinala E.K., Davies P.L., Jia Z. Crystal structure of beta-helical antifreeze protein points to a general ice binding model // Structure. 2002a. V. 10. Nо 5. P. 619–627.

80. Leinala E.K., Davies P.L., Doucet D. et al. A beta-helical antifreeze protein isoform with increased activity: structural and functional insights // J. Biol. Chem. 2002b. V. 277. P. 33349–33352.

81. Li N., Andorfer C.A., Duman J.G. Enhancement of insect antifreeze protein activity by solutes of low molecular mass // J. Exp. Biol. 1998. V. 201. P. 2243–2251.

82. Li N., Kendrick B.S., Manning M.C. et al. Secondary structure of antifreeze proteins from overwintering larvae of the beetle Dendroides canadensis // Arch. Biochem. Biophys. 1998. V. 360. P. 25–32.

83. Lin F.H., Davies P.L., Graham L.A. The Thr- and Ala-rich hyperactive antifreeze protein from inchworm folds as a fl at silk-like β-helix // Biochemistry. 2011. V. 50. Nо 21. P. 4467–4478.

84. Lin F.H., Graham L.A., Campbell R.L. et al. Structural modeling of snow fl ea antifreeze protein // Biophys. J. 2007. V. 92. Nо 5. P. 1717–1723.

85. Lin X., O’Tousa J.E., Duman J.G. Expression of two selfenhancing antifreeze proteins from the beetle Dendroides canadensis in Drosophila melanogaster // J. Insect Physiol. 2010. V. 56. Nо 4. P. 341–349.

86. Liou Y.C., Daley M.E., Graham L.A. et al. Folding and structural characterization of highly disulfide–bonded beetle antifreeze protein produced in bacteria // Protein Expr. Purif. 2000. V. 19. Nо 1. P. 148–157.

87. Liou Y.C., Thibault P., Walker V.K. et al. A complex family of highly heterogeneous and internally repetitive hyperactive antifreeze proteins from the beetle Tenebrio molitor // Biochemistry. 1999. V. 38. P. 11415–11424.

88. Liu Y., Li Z., Lin Q. et al. Structure and evolutionary origin of Ca2+–dependent herring type II antifreeze protein // PLoS ONE. 2007. V. 2. Nо 6. P. e548.

89. Mao X., Liu Z., Ma J. et al. Characterization of a novel β-helix antifreeze protein from the desert beetle Anatolica polita // Cryobiology. 2011. V. 62. Nо 2. P. 91–99.

90. Marentes E., Griffi th M., Mlynarz A. et al. Proteins accumulate in the apoplast of winter rye leaves during cold acclimation // Physiol. Plant. 1993. V. 87. P. 499–507.

91. Marshall C.B., Chakrabartty A., Davies P.L. Hyperactive antifreeze protein from winter fl ounder is a very long rodlike dimer of alpha-helices // J. Biol. Chem. 2005. V. 280. Nо 18. P. 17920–17929.

92. Marshall C.B., Daley M.E., Graham L.A. et al. Identifi cation of the ice-binding face of antifreeze protein from Tenebrio molitor // FEBS Lett. 2002. V. 529. Nо 2/3. P. 261–267.

93. Marshall C.B., Daley M.E., Sykes B.D. et al. Enhancing the activity of a beta-helical antifreeze protein by the engineered addition of coils // Biochemistry. 2004. V. 43. Nо 37. P. 11637–11646.

94. Meyer K., Keil M., Naldrett M.J. A leucine-rich repeat protein of carrot that exhibits antifreeze activity // FEBS Lett. 1999. V. 447. Nо 2/3. P. 171–178.

95. Middleton A.J., Brown A.M., Davies P.L. et al. Identifi cation of the ice-binding face of a plant antifreeze protein // FEBS Lett. 2009. V. 583. Nо 4. P. 815–819.

96. Miura K., Ohgiya S., Hoshino T. et al. Determination of the solution structure of the N-domain plus linker of Antarctic eel pout antifreeze protein RD3 // J. Biochem. 1999. V. 126. Nо 2. P. 387–394.

97. Moffatt B., Ewart V., Eastman A. Cold comfort: plant antifreeze proteins // Physiol. Plantarum. 2006. V. 126. P. 5–16.

98. Mok Y.F., Lin F.H., Graham L.A. et al. Structural basis for the superior activity of the large isoform of snow fl ea antifreeze protein // Biochemistry. 2010. V. 49. P. 2593–2603.

99. Nishimiya Y., Kondo H., Takamichi M. et al. Crystal structure and mutational analysis of Ca2+-independent type II antifreeze protein from longsnout poacher, Brachyopsis rostratus // J. Mol. Biol. 2008. V. 382. Nо 3. P. 734–746.

100. Parody-Morreale A., Murphy K.P., Di Cera E. Inhibition of bacterial ice nucleators by fi sh antifreeze glycoproteins // Nature. 1988. V. 333. P. 782–783.

101. Pertaya N., Marshall C.B., Celik Y. et al. Direct visualization of spruce budworm antifreeze protein interacting with ice crystals: basal plane affi nity confers hyperactivity // Biophys. J. 2008. V. 95. Nо 1. P. 333–341.

102. Pertaya N., Marshall C.B., DiPrinzio C.L. et al. Fluorescence microscopy evidence for quasi-permanent attachment of antifreeze proteins to ice surfaces // Biophys. J. 2007. V. 92. Nо 10. P. 3663–3673.

103. Pudney P.D., Buckley S.L., Sidebottom C.M. et al. The physicochemical characterization of a boiling stable antifreeze protein from a perennial grass (Lolium perenne) // Arch. Biochem. Biophys. 2003. V. 410. Nо 2. P. 238–245.

104. Qin W., Doucet D., Tyshenko M.G. et al. Transcription of antifreeze protein genes in Choristoneura fumiferana // Insect Mol. Biol. 2007. V. 16. Nо 4. P. 423–434.

105. Qin W., Tyshenko M.G., Doucet D. et al. Characterization of antifreeze protein gene expression in summer spruce budworm larvae // Insect Biochem. Mol. Biol. 2006. V. 36. Nо 3. P. 210–218.

106. Qin W., Walker V.K. Tenebrio molitor antifreeze protein gene identifi cation and regulation // Gene. 2006. V. 367. P. 142–149.

107. Raymond J.A., Fritsen C., Shen K. An ice-binding protein from an Antarctic sea ice bacterium // FEMS Microbiol. Ecol. 2007. V. 61. Nо 2. P. 214–221.

108. Raymond J.A., Knight C.A. Ice binding, recrystallization inhibition, and cryoprotective properties of ice–active substances associated with Antarctic sea ice diatoms // Cryobiology. 2003. V. 46. Nо 2. P. 174–181.

109. Sandve S.R., Rudi H., Asp T. et al. Tracking the evolution of a cold stress associated gene family in cold tolerant grasses // BMC Evol. Biol. 2008. V. 8. P. 245.

110. Scotter A.J., Marshall C.B., Graham L.A. et al. The basis for hyperactivity of antifreeze proteins // Cryobiology. 2006. V. 53. Nо 2. P. 229–239.

111. Smallwood M., Worrall D., Byass L. et al. Isolation and characterization of a novel antifreeze protein from carrot (Daucus carota) // Biochem. J. 1999. V. 340. Pt. 2. P. 385–391.

112. Tam R.Y., Rowley C.N., Petrov I. et al. Solution conformation of C-linked antifreeze glycoprotein analogues and modulation of ice recrystallization // J. Am. Chem. Soc. 2009. V. 131. Nо 43. P. 15745–15753.

113. Tremblay K., Ouellet F., Fournier J. et al. Molecular characterization and origin of novel bipartite cold-regulated ice recrystallization inhibition proteins from cereals // Plant Cell Physiol. 2005. V. 46. Nо 6. P. 884–891.

114. Tyshenko M.G., Doucet D., Davies P.L. et al. The antifreeze potential of the spruce budworm thermal hysteresis protein // Nat. Biotechnol. 1997. V. 15. P. 887–890.

115. Uda Y., Zepeda S., Kaneko F. et al. Adsorption-induced conformational changes of antifreeze glycoproteins at the ice/ water interface // J. Phys. Chem. B. 2007. V. 111. Nо 51. P. 14355–14361.

116. Urrutia M.E., Duman J.G., Knight C.A. Plant thermal hysteresis proteins // Biochem. Biophys. Acta. 1992. V. 1121. Nо 1/2. P. 199–206.

117. Wang S., Amornwittawat N., Juwita V. et al. Arginine, a key residue for the enhancing ability of an antifreeze protein of the beetle Dendroides canadensis // Biochemistry. 2009. V. 48. Nо 40. P. 9696–9703.

118. Wang X., DeVries A.L., Cheng C.H. Genomic basis for antifreeze peptide heterogeneity and abundance in an Antarctic eel pout: gene structures and organization // Mol. Mar. Biol. Biotechnol. 1995. V. 4. Nо 2. P. 135–147.

119. Wang L., Duman J.G. A thaumatin-like protein from larvae of the beetle Dendroides canadensis enhances the activity of antifreeze proteins // Biochemistry. 2006. V. 45. Nо 4. P. 1278–1284.

120. Wharton D.A., Barrett J., Goodall G. et al. Ice-active proteins from the Antarctic nematode Panagrolaimus davidi // Cryobiology. 2005. V. 51. Nо 2. P. 198–207.

121. Wierzbicki A., Madura J.D., Salmon C. et al. Modeling studies of binding of sea raven type II antifreeze protein to ice // J. Chem. Inf. Comput. Sci. 1997. V. 37. Nо 6. P. 1006–1010.

122. Wierzbicki A., Knight C.A., Salter E.A. et al. The role of non-polar amino acid functional groups in the surfaceorientation-dependent adsorption of natural and synthetic antifreeze peptides on ice // Crystal Growth Design. 2008. V. 8. P. 3420–3429.

123. Winfi eld M.O., Lu C., Wilson I.D., et al. Plant responses to cold: Transcriptome analysis of wheat // Plant Biotechnol. J. 2010. V. 8. Nо 7. P. 749–771.

124. Wisniewski M., Webb R., Balsamo R. et al. Purifi cation, immunolocalization, cryoprotective and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica) // Physiol. Plant. 1999. V. 105. P. 600–608.

125. Worrall D., Elias L., Ashford D. et al. A carrot leucine-richrepeat protein that inhibits ice recrystallization // Science. 1998. V. 282. Nо 5386. P. 115–117.

126. Wu Y., Banoub J., Goddard S.V. et al. 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. 2001. V. 128. Nо 2. P. 265–273.

127. Xiao N., Suzuki K., Nishimiya Y. et al. Comparison of functional properties of two fungal antifreeze proteins from Antarctomyces psychrotrophicus and Typhula ishikariensis // FEBS J. 2010. V. 277. Nо 2. P. 394–403.

128. Yaish M.W., Doxey A.C., McConkey B.J. et al. Cold–active winter rye glucanases with ice-binding capacity // Plant Physiol. 2006. V. 141. Nо 4. P. 1459–1472.

129. Yeh S., Moffatt B.A., Griffi th M. et al. Chitinase genes responsive to cold encode antifreeze proteins in winter cereals // Plant Physiol. 2000. V. 124. P. 1251–1264.

130. Yu S.O., Brown A., Middleton A.J. et al. Ice restructuring inhibition activities in antifreeze proteins with distinct differences in thermal hysteresis // Cryobiology. 2010. V. 61. P. 327–334.

131. Yu J., Cheng C.H., DeVries A.L. et al. Characterization of a multimer type III antifreeze protein gene from the Antarctic eel pout (Lycodichthys dearborni) // Yi Chuan Xue Bao. 2005. V. 32. Nо 8. P. 789–794.

132. Zachariassen K.E., DeVries A.L., Hunt B. et al. Effect of ice fraction and dilution factor on the antifreeze activity in the hemolymph of the cerambycid beetle Rhagium inquisitor // Cryobiology. 2002. V. 44. Nо 2. P. 132–141.

133. Zachariassen K.E., Kristiansen E. Ice nucleation and antinucleation in nature // Cryobiology. 2000. V. 41. Nо 4. P. 257–279.

134. Zhang J., Deng C., Wang J. et al. Identifi cation of a two-domain antifreeze protein gene in Antarctic eelpout Lycodichthys dearborni //·Polar Biology. 2009. V. 32. P. 35–40.

135. Zhang D.Q., Liu B., Feng D.R. et al. Expression, purifi cation, and antifreeze activity of carrot antifreeze protein and its mutants // Protein Expr. Purif. 2004. V. 35. Nо 2. P. 257–263.

136. Zhang D.Q., Wang H.B., Liu B. et al. Carrot antifreeze protein does not exhibit the polygalacturonase-inhibiting activity of PGIP family // Yi Chuan Xue Bao. 2006. V. 33. Nо 11. P. 1027–1036.

137. Zhang C., Zhang H., Wang L. et al. Improvement of texture properties and fl avor of frozen dough by carrot (Daucus carota) antifreeze protein supplementation // J. Agric. Food Chem. 2007. V. 55. Nо 23. P. 9620–9626.

138. Zhang C., Fei S.Z., Arora R. et al. Ice recrystallization inhibition proteins of perennial ryegrass enhance freezing tolerance // Planta. 2010. V. 232. Nо 1. P. 155–164.