Cold survival in freeze-intolerant insects: The structure and function of β-helical antifreeze proteins

European Journal of Biochemistry

Volumn 271, Issue 16, 2004, Pages 3285-3296

  Graether, Steffen P ^a,b   Sykes, Brian D ^a  

^a CANADIAN INSTITUTES OF HEALTH RESEARCH   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Antifreeze protein; Beta helix; Dynamics; Ice; Insect; NMR; Structure; Thermal hysteresis; Water; X ray crystallography

Indexed keywords

ANTIFREEZE PROTEIN; ICE; INSECT PROTEIN; THREONINE;

AMINO ACID SEQUENCE; BIOLOGICAL MODEL; COLD TOLERANCE; FREEZING TOLERANCE; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PERENNIAL RYEGRASS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SPECIES COMPARISON; STRUCTURE ACTIVITY RELATION; TENEBRIO; WORM; X RAY CRYSTALLOGRAPHY;

ACCLIMATIZATION; ANIMALS; ANTIFREEZE PROTEINS; FREEZING; INSECTS; PROTEIN CONFORMATION;

ARACHNIDA; CHORISTONEURA FUMIFERANA; DAUCUS CAROTA; HEXAPODA; INSECTA; LOLIUM; LOLIUM PERENNE; PICEA; TENEBRIO; TENEBRIO MOLITOR;

EID: 4344642832     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04256.x     Document Type: Review

References (73)

1. Storey, K.B. & Storey, J.M. (1991) Biochemistry of cryoprotectants. In Insects at Low Temperatures (Lee, R.E. & Denlinger, D., eds), pp. 64-93. Chapman & Hall, New York, USA.
2. Fletcher, G.L., Hew, C.L. & Davies, P.L. (2001) Antifreeze Proteins of Teleost Fishes. Annu. Rev. Physiol. 63, 359-390.
3. Breton, G., Danyluk, J., Ouellet, F. & Sarhan, F. (2000) Biotechnological applications of plant freezing associated proteins. Biotechnol. Annu. Rev. 6, 59-101.
4. Gilbert, J.A., Hill, P.J., Dodd, C.E.R. & Laybourn-Parry, J. (2004) Demonstration of antifreeze protein activity in Antarctic lake bacteria. Microbiology 159, 171-180.
5. Hoshino, T., Kiriaki, M., Ohgjya, S., Fujiwara, M., Kondo, H., Nishimiya, Y., Yumoto, I. & Tsuda, S. (2003) Antifreeze proteins from snow mold fungi. Can J. Bot.-Revue Can. Bot. 81, 1175-1181.
6. Duman, J.G. (2001) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu. Rev. Physiol. 63, 327-357.
7. Raymond, J.A. & DeVries, A.L. (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc. Natl Acad. Sci. USA 74, 2589-2593.
8. Wilson, P.W. & Leader, J.P. (1995) Stabilization of supercooled fluids by thermal hysteresis proteins. Biophys. J. 68, 2098-2107.
9. Davies, P.L. & Sykes, B.D. (1997) Antifreeze proteins. Curr. Opin. Struct. Biol. 7, 828-834.
10. Ewart, K.V., Lin, Q. & Hew, C.L. (1999) Structure, function and evolution of antifreeze proteins. Cell Mol. Life Sci. 55, 271-283.
11. Yeh, Y. & Feeney, R.E. (1996) Antifreeze proteins: Structures and mechanisms of function. Chem. Rev. 96, 601-617.
12. Jia, Z. & Davies, P.L. (2002) Antifreeze proteins: an unusual receptor-ligand interaction. Trends Biochem. Sci. 27, 101-106.
13. Sönnichsen, F.D., Davies, P.L. & Sykes, B.D. (1998) NMR structural studies on antifreeze proteins. Biochem. Cell Biol. 76, 284-293.
14. Tachibana, Y., Fletcher, G.L., Fujitani, N., Tsuda, S., Monde, K. & Nishimura, S.I. (2004) Antifreeze glycoproteins: elucidation of the structural motifs that are essential for antifreeze activity. Angew. Chem. Int., 43, 856-862.
15. Ben, R.N. (2001) Antifreeze glycoproteins - preventing the growth of ice. Chembiochemistry 2, 161-166.
16. Harding, M.M., Anderberg, P.I. & Haymet, A.D. (2003) 'Antifreeze' glycoproteins from polar fish. Eur. J. Biochem. 270, 1381-1392.
17. Sicheri, F. & Yang, D.S. (1995) Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature 375, 427-431.
18. Yang, D.S., Sax, M., Chakrabartty, A. & Hew, C.L. (1988) Crystal structure of an antifreeze polypeptide and its mechanistic implications. Nature 333, 232-237.
19. DeVries, A.L. & Lin, Y. (1977) Structure of a peptide antifreeze and mechanism of adsorption to ice. Biochim. Biophys. Acta 495, 388-392.
20. Knight, C.A., Cheng, C.C. & DeVries, A.L. (1991) Adsorption of alpha-helical antifreeze peptides on specific ice crystal surface planes. Biophys. J. 59, 409-418.
21. Wen, D. & Laursen, R.A. (1992) A model for binding of an antifreeze polypeptide to ice. Biophys. J. 63, 1659-1662.
22. Chao, H., Houston, M.E., Hodges, R.S., Kay, C.M., Sykes, B.D., Loewen, M.C., Davies, P.L. & Sönnichsen, F.D. (1997) A diminished role for hydrogen bonds in antifreeze protein binding to ice. Biochemistry 36, 14652-14660.
23. Haymet, A.D., Ward, L.G., Harding, M.M. & Knight, C.A. (1998) Valine substituted winter flounder 'antifreeze': preservation of ice growth hysteresis. FEBS Lett. 430, 301-306.
24. Zhang, W. & Laursen, R.A. (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, 34806-34812.
25. Baardsnes, J., Kondejewski, L.H., Hodges, R.S., Chao, H., Kay, C. & Davies, P.L. (1999) New ice-binding face for type I antifreeze protein. FEBS Lett. 463, 87-91.
26. Gronwald, W., Loewen, M.C., Lix, B., Daugulis, A.J., Sönnichsen, F.D., Davies, P.L. & Sykes, B.D. (1998) The solution structure of type II antifreeze protein reveals a new member of the lectin family. Biochemistry 37, 4712-4721.
27. Sonnichsen, F.D., DeLuca, C.I., Davies, P.L. & Sykes, B.D. (1996) Refined solution structure of type III antifreeze protein: hydrophobic groups may be involved in the energetics of the protein-ice interaction. Structure 4, 1325-1337.
28. Jia, Z., DeLuca, C.I., Chao, H. & Davies, P.L. (1996) Structural basis for the binding of a globular antifreeze protein to ice. Nature 384, 285-288.
29. Yang, D.S., Hon, W.C., Bubanko, S., Xue, Y., Seetharaman, J., Hew, C.L. & Sicheri, F. (1998) Identification of the ice-binding surface on a type III antifreeze protein with a 'flatness function' algorithm. Biophys. J. 74, 2142-2151.
30. Antson, A.A., Smith, D.J., Roper, D.I., Lewis, S., Caves, L.S., Verma, C.S., Buckley, S.L., Lillford, P.J. & Hubbard, R.E. (2001) Understanding the mechanism of ice binding by type III antifreeze proteins. J. Mol. Biol. 305, 875-889.
31. Tyshenko, M.G., Doucet, D., Davies, P.L. & Walker, V.K. (1997) The antifreeze potential of the spruce budworm thermal hysteresis protein. Nat. Biotechnol. 15, 887-890.
32. Graham, L.A., Liou, Y.C., Walker, V.K. & Davies, P.L. (1997) Hyperactive antifreeze protein from beetles. Nature 388, 727-728.
33. Andorfer, C.A. & Duman, J.G. (2000) Isolation and characterization of cDNA clones encoding antifreeze proteins of the pyrochroid beetle Dendroides canadensis. J. Insect Physiol. 46, 365-372.
34. Graether, S.P., Kuiper, M.J., Gagné, S.M., Walker, V.K., Jia, Z., Sykes, B.D. & Davies, P.L. (2000) Beta-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature 406, 325-328.
35. Wilson, P., Gould, M. & DeVries, A. (2002) Hexagonal shaped ice spicules in frozen antifreeze protein solutions. Cryobiology 44, 240.
36. Liou, Y.C., Thibault, P., Walker, V.K., Davies, P.L. & Graham, L.A. (1999) A complex family of highly heterogeneous and internally repetitive hyperactive antifreeze proteins from the beetle Tenebrio molitor. Biochemistry 38, 11415-11424.
37. Leinala, E.K., Davies, P.L. & Jia, Z. (2002) Crystal Structure of beta-Helical Antifreeze Protein Points to a General Ice Binding Model. Structure 10, 619-627.
38. Graether, S.P., Gagné, S.M., Spyracopoulos, L., Jia, Z., Davies, P.L. & Sykes, B.D. (2003) Spruce budworm antifreeze protein: changes in structure and dynamics at low temperature. J. Mol. Biol. 327, 1155-1168.
39. Liou, Y.C., Tocilj, A., Davies, P.L. & Jia, Z. (2000) Mimicry of ice structure by surface hydroxyls and water of a beta-helix antifreeze protein. Nature 406, 322-324.
40. Daley, M.E., Spyracopoulos, L., Jia, Z., Davies, P.L. & Sykes, B.D. (2002) Structure and dynamics of a beta-helical antifreeze protein. Biochemistry 41, 5515-5525.
41. Jenkins, J. & Pickersgill, R. (2001) The architecture of parallel β-helices and related folds. Prog. Biophys. Mol. Biol. 77, 111-175.
42. Gauthier, S.Y., Kay, C.M., Sykes, B.D., Walker, V.K. & Davies, P.L. (1998) Disulfide bond mapping and structural characterization of spruce budworm antifreeze protein. Eur. J. Biochem. 258, 445-453.
43. Liou, Y.C., Daley, M.E., Graham, L.A., Kay, C.M., Walker, V.K., Sykes, B.D. & Davies, P.L. (2000) Folding and structural characterization of highly disulfide-bonded beetle antifreeze protein produced in bacteria. Protein Expr. Purif. 19, 148-157.
44. Yoder, M.D., Keen, N.T. & Jurnak, F. (1993) New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science 260, 1503-1507.
45. Raetz, C.R. & Roderick, S.L. (1995) A left-handed parallel beta helix in the structure of UDP-N- acetylglucosamine acyltransferase. Science 270, 997-1000.
46. Richardson, J.S. (1976) Handedness of crossover connections in beta sheets. Proc. Natl Acad. Sci. USA 73, 2619-2623.
47. Kobe, B. & Kajava, A.V. (2000) When protein folding is simplified to protein coiling: the continuum of solenoid protein structures. Trends Biochem. Sci. 25, 509-515.
48. Lazo, N.D. & Downing, D.T. (1997) Beta-helical fibrils from a model peptide. Biochem. Biophys. Res. Commun. 235, 675-679.
49. Lazo, N.D. & Downing, D.T. (1998) Amyloid fibrils may be assembled from beta-helical protofibrils. Biochemistry 37, 1731-1735.
50. Graether, S.P., Slupsky, C.M. & Sykes, B.D. (2003) Freezing of a fish antifreeze protein results in amyloid fibril formation. Biophys. J. 84, 552-557.
51. Shindyalov, I.N. & Bourne, P.E. (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 11, 739-747.
52. Duman, J.G., Verleye, D. & Li, N. (2002) Site-specific forms of antifreeze protein in the beetle Dendroides canadensis. J. Comp. Physiol. [B] 172, 547-552.
53. Marshall, C., Daley, M., Graham, L., Sykes, B.D. & Davies, P. (2002) Identification of the ice-binding face of antifreeze protein from Tenebrio molitor. FEBS Lett. 529, 261.
54. Yang, Z., Zhou, Y., Liu, K., Cheng, Y., Liu, R., Chen, G. & Jia, Z. (2003) Computational study on the function of water within a beta-helix antifreeze protein dimer and in the process of ice-protein binding. Biophys. J. 85, 2599-2605.
55. Doucet, D., Tyshenko, M.G., Davies, P.L. & Walker, V.K. (2002) A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. Eur. J. Biochem. 269, 38-46.
56. Doucet, D., Tyshenko, M.G., Kuiper, M.J., Graether, S.P., Sykes, B.D., Daugulis, A.J., Davies, P.L. & Walker, V.K. (2000) Structure-function relationships in spruce budworm antifreeze protein revealed by isoform diversity. Eur. J. Biochem. 267, 6082-6088.
57. Leinala, E.K., Davies, P.L., Doucet, D., Tyshenko, M.G., Walker, V.K. & Jia, Z. (2002) A beta-helical antifreeze protein isoform with increased activity: structural and functional insights. J. Biol. Chem. 277, 33349-33352.
58. Marshall, C.B., Tomczak, M.M., Gauthier, S.Y., Kuiper, M.J., Lankin, C., Walker, V.K. & Davies, P.L. (2004) Partitioning of fish and insect antifreeze proteins into ice suggests they bind with comparable affinity. Biochemistry 43, 148-154.
59. Daley, M.E. & Sykes, B.D. (2003) The role of side chain conformational flexibility in surface recognition by Tenebrio molitor antifreeze protein. Protein Sci. 12, 1323-1331.
60. Daley, M.E. & Sykes, B.D. (2004) Characterization of threonine side chain dynamics in an antifreeze protein using natural abundance (13)C NMR spectroscopy. J. Biomol. NMR 29, 139-150.
61. Wen, D. & Laursen, R.A. (1993) A D-antifreeze polypeptide displays the same activity as its natural L-enantiomer. FEBS Lett. 317, 31-34.
62. Laursen, R.A., Wen, D.Y. & Knight, C.A. (1994) Enantioselective adsorption of the D-forms and 1-forms of an alpha-helical antifreeze polypeptide to the (20(-2),1) planes of ice. J. Am. Chem. Soc. 116, 12057-12058.
63. Zhang, D.Q., Liu, B., Feng, D.R., He, Y.M., Wang, S.Q., Wang, H.B. & Wang, J.F. (2004) Significance of conservative asparagine residues in the thermal hysteresis activity of carrot antifreeze protein. Biochem. J. 377, 589-595.
64. Kuiper, M.J., Davies, P.L. & Walker, V.K. (2001) A theoretical model of a plant antifreeze protein from Lolium perenne. Biophys. J. 81, 3560-3565.
65. Warren, G. & Wolber, P. (1991) Molecular aspects of microbial ice nucleation. Mol. Microbiol. 5, 239-243.
66. Gurian-Sherman, D. & Lindow, S.E. (1993) Bacterial ice nucleation: significance and molecular basis. FASEB J. 7, 1338-1343.
67. Hew, C.L. & Yang, D.S. (1992) Protein interaction with ice. Eur. J. Biochem. 203, 33-42.
68. Graether, S.P. & Jia, Z. (2001) Modeling Pseudomonas syringae ice-nucleation protein as a β-helical protein. Biophys. J. 80, 1169-1173.
69. Wolber, P. & Warren, G. (1989) Bacterial ice-nucleation proteins. Trends Biochem. Sci. 14, 179-182.
70. Hayward, J.A. & Haymet, A.D.J. (2002) The ice/water interface: orientational order parameters for the basal, prism, {2021}, and {2110} interfaces of ice Ih. Phys Chem. Chem. Physics 4, 3712-3719.
71. Breiter, D.R., Kanost, M.R., Benning, M.M., Wesenberg, G., Law, J.H., Wells, M.A., Rayment, I. & Holden, H.M. (1991) Molecular structure of an apolipoprotein determined at 2.5-A resolution. Biochemistry 30, 603-608.
72. Kraulis, P.J. (1991) MOLSCRIPT - A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
73. Merritt, E.A. & Bacon, D.J. (1997) Raster3D: Photorealistic molecular graphics. Macromolecular Crystallogr., Part B 277, 505-524.