Characterization of the ice-binding protein from Arctic yeast Leucosporidium sp. AY30

Cryobiology

Volumn 64, Issue 3, 2012, Pages 286-296

  Park, Kyoung Sun ^a   Do, Hackwon ^a   Lee, Jun Hyuck ^a   Park, Seung Il ^b   Kim, Eun jung ^a   Kim, Soon Jong ^c   Kang, Sung Ho ^a   Kim, Hak Jun ^a  

^a Korea Polar Research Institute (KOPRI)   (South Korea)

^b Korea Research Institute of Ships and Ocean Engineering   (South Korea)

^c Mokpo National University   (South Korea)

Author keywords

Ice binding protein; Leucosporidium sp.; N linked glycosylation; Reversible dimer; Thermal hysteresis

Indexed keywords

BINDING PROTEIN; ICE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYSTALLIZATION; GEL PERMEATION CHROMATOGRAPHY; LEUCOSPORIDIUM; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS; THERMAL ANALYSIS; ULTRACENTRIFUGATION; YEAST;

ANTIFREEZE PROTEINS; ARCTIC REGIONS; BASIDIOMYCOTA; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; CLONING, MOLECULAR; CRYSTALLIZATION; DIMERIZATION; ESCHERICHIA COLI; FREEZING; FUNGAL PROTEINS; GLYCOSYLATION; ICE; KINETICS; MODELS, MOLECULAR; PICHIA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS; SPECTROMETRY, FLUORESCENCE; ULTRACENTRIFUGATION;

LEUCOSPORIDIUM;

EID: 84862807174     PISSN: 00112240     EISSN: 10902392     Source Type: Journal    
DOI: 10.1016/j.cryobiol.2012.02.014     Document Type: Article

References (61)

1. Achenbach J.C., Ewart K.V. Structural and functional characterization of a C type lectin like antifreeze protein from rainbow smelt (Osmerus mordax). Eur. J. Biochem. 2002, 269:1219-1226.
2. Achenbach J.C., Ewart K.V. Structural and functional characterization of a C-type lectin-like antifreeze protein from rainbow smelt (Osmerus mordax). Eur. J. Biochem. 2002, 269:1219-1226.
3. 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. Understanding the mechanism of ice binding by type III antifreeze proteins. J. Mol. Biol. 2001, 305:875-889.
4. Bayer-Giraldi M., Uhlig C., John U., Mock T., Valentin K. Antifreeze proteins in polar sea ice diatoms: diversity and gene expression in the genus Fragilariopsis. Environ. Microbiol. 2010, 12:1041-1052.
5. Bayer-Giraldi M., Weikusat I., Besir H., Dieckmann G. Characterization of an antifreeze protein from the polar diatom Fragilariopsis cylindrus and its relevance in sea ice. Cryobiology 2011, 63:210-219.
6. Bohm G., Muhr R., Jaenicke R. Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng. 1992, 5:191-195.
7. DeLuca C.I., Comley R., Davies P.L. Antifreeze proteins bind independently to ice. Biophys. J. 1998, 74:1502-1508.
8. Devries A.L. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 1971, 172:1152.
9. DeVries A.L. Antifreeze glycopeptides and peptides: interactions with ice and water. Methods Enzymol. 1986, 127:293-303.
10. Doucet D., Tyshenko M.G., Davies P.L., Walker V.K. A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. Eur. J. Biochem. 2002, 269:38-46.
11. Duman J.G. Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara. Biochim. Biophys. Acta 1994, 1206:129-135.
12. Duman J.G., Olsen T.M. Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 1993, 30:322-328.
13. Duman J.G., Bennett V., Sformo T., Hochstrasser R., Barnes B.M. Antifreeze proteins in Alaskan insects and spiders. J. Insect Physiol. 2004, 50:259-266.
14. Ewart K.V., Lin Q., Hew C.L. Structure, function and evolution of antifreeze proteins. Cell. Mol. Life Sci. 1999, 55:271-283.
15. Fletcher G.L., Hew C.L., Davies P.L. Antifreeze proteins of teleost fishes. Annu. Rev. Physiol. 2001, 63:359-390.
16. Garnham C.P., Gilbert J.A., Hartman C.P., Campbell R.L., Laybourn-Parry J., Davies P.L. A Ca2+-dependent bacterial antifreeze protein domain has a novel β-helical ice-binding fold. Biochem. J. 2008, 411:171-180.
17. Gilbert J.A., Davies P.L., Laybourn-Parry J. A hyperactive, Ca2+-dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiol. Lett. 2005, 245:67-72.
18. Graether S.P., Kuiper M.J., Gagne S.M., Walker V.K., Jia Z., Sykes B.D., Davies P.L. β-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature 2000, 406:325-328.
19. Graham L.A., Davies P.L. Glycine-rich antifreeze proteins from snow fleas. Science 2005, 310:461.
20. Graham L.A., Liou Y.C., Walker V.K., Davies P.L. Hyperactive antifreeze protein from beetles. Nature 1997, 388:727-728.
21. Graham L.A., Marshall C.B., Lin F.H., Campbell R.L., Davies P.L. Hyperactive antifreeze protein from fish contains multiple ice-binding sites. Biochemistry 2008, 47:2051-2063.
22. Griffith M., Yaish M.W. Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci. 2004, 9:399-405.
23. Griffith M., Ala P., Yang D.S., Hon W.C., Moffatt B.A. Antifreeze protein produced endogenously in winter rye leaves. Plant Physiol. 1992, 100:593-596.
24. Hoshino T., Kiriaki M., Ohgiya S., Fujiwara M., Kondo H., Nishimiya Y., Yumoto I., Tsuda S. Antifreeze proteins from snow mold fungi. Can. J. Bot. 2003, 81:1175-1181.
25. Huang T., Nicodemus J., Zarka D.G., Thomashow M.F., Wisniewski M., Duman J.G. Expression of an insect (Dendroides canadensis) antifreeze protein in Arabidopsis thaliana results in a decrease in plant freezing temperature. Plant Mol. Biol. 2002, 50:333-344.
26. Janech M., Krell A., Mock T., Kang J.-S., Raymond J.A. Ice-binding proteins from sea ice diatoms (bacillariophyceae). J. Phycol. 2006, 42:410-416.
27. Jia Z., Davies P.L. Antifreeze proteins: an unusual receptor-ligand interaction. Trends Biochem. Sci. 2002, 27:101-106.
28. Kawahara H., Nakano Y., Omiya K., Muryoi N., Nishikawa J., Obata H. Production of two types of ice crystal-controlling proteins in Antarctic bacterium. J. Biosci. Bioeng. 2004, 98:220-223.
29. Kawahara H., Iwanaka Y., Higa S., Muryoi N., Sato M., Honda M., Omura H., Obata H. A novel, intracellular antifreeze protein in an antarctic bacterium, Flavobacterium xanthum. Cryo Lett. 2007, 28:39-49.
30. Knight C.A., Cheng C.C., DeVries A.L. Adsorption of α-helical antifreeze peptides on specific ice crystal surface planes. Biophys. J. 1991, 59:409-418.
31. Knott G.D. Comput. Programs Biomed. 1979, 10:271-280.
32. Krell A., Beszteri B., Dieckmann G., Glöckner G., Valentin K., Mock T. A new class of ice-binding proteins discovered in a salt-stress-induced cDNA library of the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). Eur. J. Phycol. 2008, 43:423-433.
33. Kuiper M.J., Lankin C., Gauthier S.Y., Walker V.K., Davies P.L. Purification of antifreeze proteins by adsorption to ice. Biochem. Biophys. Res. Commun. 2003, 300:645-648.
34. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
35. T.M. Laue, B.D. Shah, T.M. Ridgeway, S.L. Pelletier, Computer-aided interpretation of analytical sedimentation data for proteins, in: S.E. Harding et al. (Eds.), Analytical ultracentrifugation in biochemistry and polymer science, 1992, pp. 90-125.
36. Lee J.K., Park K.S., Park S., Park H., Song Y.H., Kang S.H., Kim H.J. An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 2010, 60:222-228.
37. Leinala E.K., Davies P.L., Jia Z. Crystal structure of β-helical antifreeze protein points to a general ice binding model. Structure 2002, 10:619-627.
38. Li Z., Xiong F., Lin Q., d'Anjou M., Daugulis A.J., Yang D.S., Hew C.L. Low-temperature increases the yield of biologically active herring antifreeze protein in Pichia pastoris. Protein Exp. Purif. 2001, 21:438-445.
39. Lin F.H., Davies P.L., Graham L.A. The Thr- and Ala-rich hyperactive antifreeze protein from inchworm folds as a flat silk-like β-helix. Biochemistry 2011, 50:4467-4478.
40. Liou Y.C., Thibault P., Walker V.K., Davies P.L., Graham L.A. A complex family of highly heterogeneous and internally repetitive hyperactive antifreeze proteins from the beetle Tenebrio molitor. Biochemistry 1999, 38:11415-11424.
41. Mao X., Liu Z., Ma J., Pang H., Zhang F. Characterization of a novel β-helix antifreeze protein from the desert beetle Anatolica polita. Cryobiology 2011, 62:91-99.
42. Marshall C.B., Daley M.E., Graham L.A., Sykes B.D., Davies P.L. Identification of the ice-binding face of antifreeze protein from Tenebrio molitor. FEBS Lett. 2002, 529:261-267.
43. Marshall C.B., Chakrabartty A., Davies P.L. Hyperactive antifreeze protein from winter flounder is a very long rod-like dimer of β-helices. J. Biol. Chem. 2005, 280:17920.
44. Marshall C.B., Chakrabartty A., Davies P.L. Hyperactive antifreeze protein from winter flounder is a very long rod-like dimer of α-helices. J. Biol. Chem. 2005, 280:17920-17929.
45. Mok Y.F., Lin F.H., Graham L.A., Celik Y., Braslavsky I., Davies P.L. Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry 2010, 49:2593-2603.
46. Park A.K., Park K.S., Kim H.J., Park H., Ahn I.Y., Chi Y.M., Moon J.H. Crystallization and preliminary X-ray crystallographic studies of the ice-binding protein from the Antarctic yeast Leucosporidium sp. AY30. Acta Cryst. 2011, F67:800-802.
47. Raymond J.A., Janech M.G. Ice-binding proteins from enoki and shiitake mushrooms. Cryobiology 2009, 58:151-156.
48. Raymond J.A., Fritsen C., Shen K. An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol. Ecol. 2007, 61:214-221.
49. Raymond J.A., Christner B.C., Schuster S.C. A bacterial ice-binding protein from the Vostok ice core. Extremophiles 2008, 12:713-717.
50. Raymond J.A., Janech M., Fritsen C. Novel ice-binding proteins from a psychrophilic antarctic alga (chlamydomonadaceae, chlorophyceae). J. Phycol. 2009, 45:130-136.
51. Roth J., Zuber C., Park S., Jang I., Lee Y., Kysela K.G., Fourn V.L., Santimaria R., Guhl B., Cho J.W. Protein N-glycosylation, protein folding, and protein quality control. Mol. Cells 2010, 30:497-506.
52. J. Sambrook, E.F. Fritsch, T. Maniatis, Molecular Cloning: A Laboratory Manual, 1989.
53. Scotter A.J., Marshall C.B., Graham L.A., Gilbert J.A., Garnham C.P., Davies P.L. The basis for hyperactivity of antifreeze proteins. Cryobiology 2006, 53:229-239.
54. Smallwood M., Worrall D., Byass L., Elias L., Ashford D., Doucet C.J., Holt C., Telford J., Lillford P., Bowles D.J. Isolation and characterization of a novel antifreeze protein from carrot (Daucus carota). Biochem. J. 1999, 340:385-391.
55. Tomchaney A.P., Morris J.P., Kang S.H., Duman J.G. Purification, composition, and physical properties of a thermal hysteresis " antifreeze" protein from larvae of the beetle, Tenebrio molitor. Biochemistry 1982, 21:716-721.
56. Tyshenko M.G., Doucet D., Davies P.L., Walker V.K. The antifreeze potential of the spruce budworm thermal hysteresis protein. Nat. Biotechnol. 1997, 15:887-890.
57. Uhlig C., Kabisch J., Palm G.J., Valentin K., Schweder T., Krell A. Heterologous expression, refolding and functional characterization of two antifreeze proteins from Fragilariopsis cylindrus (Bacillariophyceae). Cryobiology 2011, 63:220-228.
58. Urrutia M.E., Duman J.G., Knight C.A. Plant thermal hysteresis proteins. Biochim. Biophys. Acta 1992, 1121:199-206.
59. Wang X., DeVries A.L., Cheng C.H. 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 1995, 1247:163-172.
60. Worrall D., Elias L., Ashford D., Smallwood M., Sidebottom C., Lillford P., Telford J., Holt C., Bowles D. A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 1998, 282:115.
61. Xiao N., Suzuki K., Nishimiya Y., Kondo H., Miura A., Tsuda S., Hoshino T. Comparison of functional properties of two fungal antifreeze proteins from Antarctomyces psychrotrophicus and Typhula ishikariensis. FEBS J. 2010, 277:394-403.