The Thr- and ala-rich hyperactive antifreeze protein from inchworm folds as a flat silk-like β-Helix

Biochemistry

Volumn 50, Issue 21, 2011, Pages 4467-4478

  Lin, Feng Hsu ^a   Davies, Peter L ^a   Graham, Laurie A ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFREEZE PROTEIN; CDNA SEQUENCE; FREEZING-POINT DEPRESSION; HYDROPHOBIC CORE; OXYGEN ATOM; REGULAR ARRAY;

SILK;

PROTEINS;

ALANINE; ANTIFREEZE PROTEIN; COMPLEMENTARY DNA; THREONINE;

ARTICLE; BEETLE; BETA SHEET; BINDING SITE; DNA SEQUENCE; HYDROPHOBICITY; LARVA; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DATABASE; PROTEIN FOLDING; PROTEIN STRUCTURE;

ALANINE; AMINO ACID SEQUENCE; ANIMALS; ANTIFREEZE PROTEINS; BASE SEQUENCE; CHROMATOGRAPHY, AFFINITY; CIRCULAR DICHROISM; DNA PRIMERS; DNA, COMPLEMENTARY; EXPRESSED SEQUENCE TAGS; LARVA; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MOTHS; POLYMERASE CHAIN REACTION; PROTEIN FOLDING; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; THREONINE;

CAMPAEA PERLATA; COLEOPTERA; GEOMETRIDAE; LEPIDOPTERA; RHAGIUM INQUISITOR;

EID: 79958111892     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2003108     Document Type: Article

References (64)

1. Jia, Z., and Davies, P. L. (2002) Antifreeze proteins: An unusual receptor-ligand interaction. Trends Biochem. Sci. 27, 101-106. (Pubitemid 34164326)
2. Raymond, J. A. (2000) Distribution and partial characterization of ice-active molecules associated with sea-ice diatoms. Polar Biol. 23, 721-729.
3. Kuiper, M. J., Lankin, C., Gauthier, S. Y., Walker, V. K., and Davies, P. L. (2003) Purification of antifreeze proteins by adsorption to ice. Biochem. Biophys. Res. Commun. 300, 645-648. (Pubitemid 36268884)
4. Knight, C. A., Cheng, C. C., and DeVries, A. L. (1991) Adsorption of R-helical antifreeze peptides on specific ice crystal surface planes. Biophys. J. 59, 409-418.
5. Zhang, C., Zhang, H., Wang, L., Zhang, J., and Yao, H. (2007) Purification of antifreeze protein from wheat bran (Triticum aestivum L.) based on its hydrophilicity and ice-binding capacity. J. Agric. Food Chem. 55, 7654-7658. (Pubitemid 47522168)
6. Raymond, J. A., Fritsen, C., and Shen, K. (2007) An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol. Ecol. 61, 214-221. (Pubitemid 47083943)
7. Graham, L. A., and Davies, P. L. (2005) Glycine-rich antifreeze proteins from snow fleas. Science 310, 461. (Pubitemid 41507952)
8. Duman, J. G. (2001) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu. Rev. Physiol. 63, 327-357. (Pubitemid 32304321)
9. Fletcher, G. L., Hew, C. L., and Davies, P. L. (2001) Antifreeze proteins of teleost fishes. Annu. Rev. Physiol. 63, 359-390. (Pubitemid 32304322)
10. Celik, Y., Graham, L. A., Mok, Y. F., Bar, M., Davies, P. L., and Braslavsky, I. (2010) Superheating of ice crystals in antifreeze protein solutions. Proc. Natl. Acad. Sci. U.S.A. 107, 5423-5428.
11. Knight, C. A., DeVries, A. L., and Oolman, L. D. (1984) Fish antifreeze protein and the freezing and recrystallization of ice. Nature 308, 295-296. (Pubitemid 14132040)
12. Chen, L., DeVries, A. L., and Cheng, C. H. (1997) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc. Natl. Acad. Sci. U.S.A. 94, 3811-3816. (Pubitemid 27180454)
13. DeVries, A. L., and Wohlschlag, D. E. (1969) Freezing resistance in some Antarctic fishes. Science 163, 1073-1075.
14. Sicheri, F., and Yang, D. S. (1995) Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature 375, 427-431.
15. Graether, S. P., Kuiper, M. J., Gagne, S. M., Walker, V. K., Jia, Z., Sykes, B. D., and Davies, P. L. (2000) β-Helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature 406, 325-328. (Pubitemid 30604413)
16. Pentelute, B. L., Gates, Z. P., Tereshko, V., Dashnau, J. L., Vanderkooi, J.M., Kossiakoff, A. A., and Kent, S. B. (2008) X-ray structure of snow flea antifreeze protein determined by racemic crystallization of synthetic protein enantiomers. J. Am. Chem. Soc. 130, 9695-9701.
17. Scott, G. K., Fletcher, G. L., and Davies, P. L. (1986) Fish Antifreeze Proteins: Recent Gene Evolution. Can. J. Fish. Aquat. Sci. 43 (5), 1028-1034.
18. Cheng, C. H. (1998) Evolution of the diverse antifreeze proteins. Curr. Opin. Genet. Dev. 8, 715-720.
19. Devries, A. L., and Lin, Y. (1977) Structure of a peptide antifreeze and mechanism of adsorption to ice. Biochim. Biophys. Acta 495, 388-392. (Pubitemid 8226638)
20. Sonnichsen, F. D., DeLuca, C. I., Davies, P. L., and 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. (Pubitemid 26420501)
21. Chao, H., Houston, M. E., Jr., Hodges, R. S., Kay, C. M., Sykes, B. D., Loewen, M. C., Davies, P. L., and Sonnichsen, F. D. (1997) A diminished role for hydrogen bonds in antifreeze protein binding to ice. Biochemistry 36, 14652-14660. (Pubitemid 27524385)
22. Haymet, A. D., Ward, L. G., Harding, M. M., and Knight, C. A. (1998) Valine substituted winter flounder 'antifreeze': Preservation of ice growth hysteresis. FEBS Lett. 430, 301-306. (Pubitemid 28337933)
23. Nutt, D. R., and Smith, J. C. (2008) Dual function of the hydration layer around an antifreeze protein revealed by atomistic molecular dynamics simulations. J. Am. Chem. Soc. 130, 13066-13073.
24. Modig, K., Qvist, J., Marshall, C. B., Davies, P. L., and Halle, B. (2010) High water mobility on the ice-binding surface of a hyperactive antifreeze protein. Phys. Chem. Chem. Phys. 12, 10189-10197.
25. Davies, P. L., Baardsnes, J., Kuiper, M. J., and Walker, V. K. (2002) Structure and function of antifreeze proteins. Philos. Trans. R. Soc. London, Ser. B 357, 927-935. (Pubitemid 34829659)
26. Marshall, C. B., Chakrabartty, A., and Davies, P. L. (2005) Hyperactive antifreeze protein from winter flounder is a very long rodlike dimer of R-helices. J. Biol. Chem. 280, 17920-17929. (Pubitemid 41389033)
27. Kuiper, M. J., Davies, P. L., and Walker, V. K. (2001) A theoretical model of a plant antifreeze protein from Lolium perenne. Biophys. J. 81, 3560-3565. (Pubitemid 33111499)
28. Lin, F. H., Graham, L. A., Campbell, R. L., and Davies, P. L. (2007) Structural modeling of snow flea antifreeze protein. Biophys. J. 92, 1717-1723. (Pubitemid 46393482)
29. Garnham, C. P., Gilbert, J. A., Hartman, C. P., Campbell, R. L., Laybourn-Parry, J., and Davies, P. L. (2008) A Ca2?-dependent bacterial antifreeze protein domain has a novel β-helical ice-binding fold. Biochem. J. 411, 171-180. (Pubitemid 351482359)
30. Chakrabartty, A., and Hew, C. L. (1991) The effect of enhanced R-helicity on the activity of a winter flounder antifreeze polypeptide. Eur. J. Biochem. 202, 1057-1063.
31. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSIBLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. (Pubitemid 27359211)
32. Ratnasingham, S., and Hebert, P. D. (2007) bold: The Barcode of Life Data System (http://www.barcodinglife.org). Mol. Ecol. Notes 7, 355-364. (Pubitemid 46714172)
33. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
34. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447.
35. Liou, Y. C., Daley, M. E., Graham, L. A., Kay, C. M., Walker, V. K., Sykes, B. D., and Davies, P. L. (2000) Folding and structural characterization of highly disulfide-bonded beetle antifreeze protein produced in bacteria. Protein Expression Purif. 19, 148-157. (Pubitemid 30387906)
36. Mok, Y. F., Lin, F. H., Graham, L. A., Celik, Y., Braslavsky, I., and Davies, P. L. (2010) Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry 49, 2593-2603.
37. Gauthier, S. Y., Kay, C. M., Sykes, B. D., Walker, V. K., and Davies, P. L. (1998) Disulfide bond mapping and structural characterization of spruce budworm antifreeze protein. Eur. J. Biochem. 258, 445-453. (Pubitemid 28557909)
38. Liou, Y. C., Tocilj, A., Davies, P. L., and Jia, Z. (2000) Mimicry of ice structure by surface hydroxyls and water of a β-helix antifreeze protein. Nature 406, 322-324. (Pubitemid 30604412)
39. Graham, L. A., Liou, Y. C.,Walker, V. K., andDavies, P. L. (1997) Hyperactive antifreeze protein from beetles. Nature 388, 727-728.
40. Duman, J. G., Li, N., Verleye, D., Goetz, F. W., Wu, D. W., Andorfer, C. A., Benjamin, T., and Parmelee, D. C. (1998) Molecular characterization and sequencing of antifreeze proteins from larvae of the beetle Dendroides canadensis. J. Comp. Physiol., B 168, 225-232. (Pubitemid 28203001)
41. Liou, Y. C., Thibault, P., Walker, V. K., Davies, P. L., and 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.
42. Andorfer, C. A., and 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. (Pubitemid 30123531)
43. Asakura, T., and Yao, J. (2002) 13C CP/MAS NMR study on structural heterogeneity in Bombyx mori silk fiber and their generation by stretching. Protein Sci. 11, 2706-2713. (Pubitemid 35191144)
44. Lin, Y., and Long, D. J. (1980) Purification and characterization of winter flounder antifreeze peptide messenger ribonucleic acid. Biochemistry 19, 1111-1116.
45. Hayes, P. H., Scott, G. K., Ng, N. F., Hew, C. L., and Davies, P. L. (1989) Cystine-rich type II antifreeze protein precursor is initiated from the third AUGcodon of itsmRNA. J. Biol. Chem. 264, 18761-18767. (Pubitemid 19277626)
46. Davies, P. L., Roach, A. H., and Hew, C. L. (1982) DNA sequence coding for an antifreeze protein precursor from winter flounder. Proc. Natl. Acad. Sci. U.S.A. 79, 335-339. (Pubitemid 12137712)
47. Hsiao, K. C., Cheng, C. H., Fernandes, I. E., Detrich, H. W., and DeVries, A. L. (1990) An antifreeze glycopeptide gene from the antarctic cod Notothenia coriiceps neglecta encodes a polyprotein of high peptide copy number. Proc. Natl. Acad. Sci. U.S.A. 87, 9265-9269. (Pubitemid 120030606)
48. Pertaya, N., Marshall, C. B., DiPrinzio, C. L., Wilen, L., Thomson, E. S., Wettlaufer, J. S., Davies, P. L., and Braslavsky, I. (2007) Fluorescence microscopy evidence for quasi-permanent attachment of antifreeze proteins to ice surfaces. Biophys. J. 92, 3663-3673. (Pubitemid 46698655)
49. Ravulapalli, R., Campbell, R. L., Gauthier, S. Y., Dhe-Paganon, S., and Davies, P. L. (2009) Distinguishing between calpain heterodimerization and homodimerization. FEBS J. 276, 973-982.
50. DeLuca, C. I., Comley, R., and Davies, P. L. (1998) Antifreeze proteins bind independently to ice. Biophys. J. 74, 1502-1508. (Pubitemid 28108558)
51. Graham, L. A., Marshall, C. B., Lin, F. H., Campbell, R. L., and Davies, P. L. (2008) Hyperactive antifreeze protein from fish contains multiple ice-binding sites. Biochemistry 47, 2051-2063. (Pubitemid 351287131)
52. Liou, Y. C., Daley, M. E., Graham, L. A., Kay, C. M., Walker, V. K., Sykes, B. D., and Davies, P. L. (2000) Folding and structural characterization of highly disulfide-bonded beetle antifreeze protein produced in bacteria. Protein Expression Purif. 19, 148-157. (Pubitemid 30387906)
53. Zhou, C. Z., Confalonieri, F., Medina, N., Zivanovic, Y., Esnault, C., Yang, T., Jacquet, M., Janin, J., Duguet, M., Perasso, R., and Li, Z. G. (2000) Fine organization of Bombyx mori fibroin heavy chain gene. Nucleic Acids Res. 28, 2413-2419. (Pubitemid 30349048)
54. Takahashi, Y., Gehoh, M., and Yuzuriha, K. (1999) Structure refinement and diffuse streak scattering of silk (Bombyx mori). Int. J. Biol. Macromol. 24, 127-138. (Pubitemid 29227194)
55. Fossey, S. A., Nemethy, G., Gibson, K. D., and Scheraga, H. A. (1991) Conformational energy studies of β-sheets of model silk fibroin peptides. I. Sheets of poly(Ala-Gly) chains. Biopolymers 31, 1529-1541.
56. Lotz, B., and Colonna Cesari, F. (1979) The chemical structure and the crystalline structures of Bombyx mori silk fibroin. Biochimie 61, 205-214.
57. Suzuki, Y., Okonogi, M., Yamauchi, K., Kurosu, H., Tansho, M., Shimizu, T., Saito, H., and Asakura, T. (2007) High-field 1H MAS and 15N CP-MAS NMR studies of alanine tripeptides and oligomers: Distinction of antiparallel and parallel β-sheet structures and two crystallographically independent molecules. J. Phys. Chem. B 111, 9172-9178. (Pubitemid 47317501)
58. Kristiansen, E., Ramlov, H., Hojrup, P., Pedersen, S. A., Hagen, L., and Zachariassen, K. E. (2011) Structural characteristics of a novel antifreeze protein from the longhorn beetle Rhagium inquisitor. Insect Biochem. Mol. Biol. 41, 109-117.
59. Leinala, E. K., Davies, P. L., Doucet, D., Tyshenko, M. G., Walker, V. K., and Jia, Z. (2002) A β-helical antifreeze protein isoform with increased activity. Structural and functional insights. J. Biol. Chem. 277, 33349-33352. (Pubitemid 34984858)
60. Marshall, C. B., Daley, M. E., Sykes, B. D., and Davies, P. L. (2004) Enhancing the activity of a β-helical antifreeze protein by the engineered addition of coils. Biochemistry 43, 11637-11646. (Pubitemid 39277609)
61. Walters, K. R., Serianni, A. S., Sformo, T., Barnes, B. M., and Duman, J. G. (2009) A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. Proc. Natl. Acad. Sci. U.S.A. 106, 20210-20215.
62. Tomchaney, A. P., Morris, J. P., Kang, S. H., and Duman, J. G. (1982) Purification, composition, and physical properties of a thermal hysteresis "antifreeze" protein from larvae of the beetle Tenebrio molitor. Biochemistry 21, 716-721.
63. Tyshenko, M. G., Doucet, D., Davies, P. L., and Walker, V. K. (1997) The antifreeze potential of the spruce budworm thermal hysteresis protein. Nat. Biotechnol. 15, 887-890. (Pubitemid 27391783)
64. Scotter, A. J., Marshall, C. B., Graham, L. A., Gilbert, J. A., Garnham, C. P., and Davies, P. L. (2006) The basis for hyperactivity of antifreeze proteins. Cryobiology 53, 229-239. (Pubitemid 44353458)