Purification, crystal structure determination and functional characterization of type III antifreeze proteins from the European eelpout Zoarces viviparus

Cryobiology

Volumn 69, Issue 1, 2014, Pages 163-168

  Wilkens, Casper ^a,c   Poulsen, Jens Christian N ^a   Ramløv, Hans ^b   Lo Leggio, Leila ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b ROSKILDE UNIVERSITY   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Antifreeze protein; Crystal structure; Dimerization; Protein purification; Zoarces viviparus

Indexed keywords

ANTIFREEZE PROTEIN; DIMER; ISOPROTEIN; UNCLASSIFIED DRUG; ZVAFP13 PROTEIN; ZVAFP6 PROTEIN;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIMERIZATION; ELECTROPHORESIS; FISH; GEL FILTRATION; NEUTRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; ZOARCES VIVIPARUS; ADAPTATION; AMINO ACID SEQUENCE; ANIMAL; COLD; GENETICS; METABOLISM; MOLECULAR GENETICS; PERCIFORMES; SEQUENCE ALIGNMENT; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

ZOARCES VIVIPARUS; ZOARCIDAE;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; ANTIFREEZE PROTEINS, TYPE III; COLD TEMPERATURE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; MOLECULAR SEQUENCE DATA; PERCIFORMES; PROTEIN ISOFORMS; SEQUENCE ALIGNMENT;

EID: 84905908220     PISSN: 00112240     EISSN: 10902392     Source Type: Journal    
DOI: 10.1016/j.cryobiol.2014.07.003     Document Type: Article

References (32)

1. Albers C.N., Bjorn-Mortensen M., Hansen P.F., Ramløv H., Sorensen T.F. Purification and structural analysis of a type III antifreeze protein from the European eelpout Zoarces viviparus. Cryo. Lett. 2007, 28:51-60.
2. Baardsnes J., Davies P.L. Contribution of hydrophobic residues to ice binding by fish type III antifreeze protein. Biochim. Biophys. Acta 2002, 1601:49-54.
3. Chen V.B., Arendall B., Headd J.J., Keedy D.A., Immormino R.M., Kapral G.J., Murray L.W., Richardson J.S., Richardson D.C. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. 2010, D66:12-21.
4. Cheng C.-H.C., DeVries A.L. Structures of antifreeze peptides from the Antarctic eel pout, Austrolycicthys brachycephalus. Biochim. Biophys. Acta 1989, 997:55-64.
5. DeLuca C.I., Davies P.L., Ye Q., Jia Z. The effects of steric mutations on the structure of type III antifreeze protein and its interaction with ice. J. Mol. Biol. 1998, 275:515-525.
6. DeLuca C.I., Chao H., Sönnichsen F.D., Sykes B.D., Davies P.L. Effect of type III antifreeze protein dilution and mutation on the growth inhibition of ice. Biophys. J. 1996, 71:2346-2355.
7. Duman J.G. Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu. Rev. Physiol. 2001, 63:327-357.
8. Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallogr. 2010, D53:486-501.
9. Fletcher G.L., Hew C.L., Davies P.L. Antifreeze proteins of teleost fishes. Annu. Rev. Physiol. 2001, 63:359-390.
10. Garnham C.P., Nishimiya Y., Tsuda S., Davies P.L. Engineering a naturally inactive isoform of type III antifreeze protein into one that stop the growth of ice. FEBS Lett. 2012, 586:3876-3881.
11. Garnham C.P., Natarajan A., Middleton A.J., Kuiper M.J., Braslavsky I., Davies P.L. Compound ice-binding site of an antifreeze protein revealed by mutagenesis and fluorescent tagging. Biochemistry 2010, 49:9063-9071.
12. Gallagher K.R., Sharp K.A. Analysis of thermal hysteresis protein hydration using the random network model. Biophys. Chem. 2003, 105:195-209.
13. Graether S.P., DeLuca C.I., Baardsnes J., Hill G.A., Davies P.L., Jia Z. Quantitative and qualitative analysis of type III antifreeze protein structure and function. J. Biol. Chem. 1999, 274:11842-11847.
14. Howard E.I., Blakeley M.P., Haertlein M., Petit-Haertlein I., Mitschler A., Fischer S.J., Cousido-Siah A., Salvay A.G., Popov A., Muller-Dieckmann C., Petrova T., Podjarny A. Neutron structure of type-III antifreeze protein allows the reconstruction of AFP-ice interface. J. Mol. Recognit. 2011, 24:724-732.
15. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 1993, 26:795-800.
16. Katoh K., Frith M.C. Adding unaligned sequences into an existing alignment using MAFFT and LAST. Bioinformatics 2012, 28:3144-3146.
17. Ko T.-P., Robinson H., Gao Y.-G., Cheng C.-H.G., DeVries A.L., Wang A.H.-J. The refined crystal structure of an eel pout type III antifreeze protein RD1 at 0.62-Å resolution reveals structural microheterogeneity of protein and salvation. Biophys. J. 2003, 84:1228-1237.
18. Krissinel E., Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372:774-797.
19. Li J.-Y., Cui Y.-M., Chen L.-L., Gu M., Li J., Nan F.-J., Ye Q.-Z. Mutations at the S1 sites of methionine aminopeptidases from Escherichia coli and Homo sapiens reveal the residues critical for substrate specificity. J. Biol. Chem. 2004, 279:21128-21134.
20. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. 1997, D53:240-255.
21. Nishimiya Y., Sato R., Takamichi M., Miura A., Tsuda S. Co-operative effect of the isoforms of type III antifreeze protein expressed in Notched-fin eelpout, Zoarces elongatus Kner. FEBS J. 2005, 272:482-492.
22. Ramlov H. Aspects of natural cold tolerance in ectothermic animals. Hum. Reprod. 2000, 15:26-46.
23. Ramløv H. Measuring antifreeze activity. Biochemistry and Function of Antifreeze Proteins 2010, 7-42. Nova Science Publishers Inc., New York. S.P. Graether (Ed.).
24. Raymond J.A., DeVries A.L. Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc. Natl. Acad. Sci. U.S.A. 1977, 74:2589-2593.
25. Siemer A.B., Huamg K.-Y., Mcdermott A.E. Protein-ice interaction of and antifreeze protein observed with solid-state NMR. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17580-17585.
26. Smolin N., Dagett V. Formation of ice-like water structure on the surface of an antifreeze protein. J. Phys. Chem. B 2008, 112:6193-6202.
27. Sørensen T.F., Cheng C.H., Ramløv H. Isolation and some characterization of antifreeze protein from European eelpout Zoarces viviparus. Cryo. Lett. 2006, 27:387-399.
28. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 1997, 30:1022-1025.
29. Wang X., DeVries A.L., Cheng C.-H.C. 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.
30. Wilson P.W. Explaining thermal hysteresis by the Kelvin effect. Cryo. Lett. 1993, 14:31-36.
31. Yang C., Sharp K.A. The mechanism of the type III antifreeze protein action: a computational study. Biophys. Chem. 2004, 109:137-148.
32. Yang D.S., Hon W.C., Bubanko S., Xue Y., Seetharaman J., Hew C.L., Sicheri F. Identification of the ice-binding surface on a type III antifreeze protein with a "flatness function" algorithm. Biophys. J. 1998, 74:2142-2151.