References
Antson AA, Smith DJ, Roper DI, Lewis S, Caves LS, Verma CS, Buckley SL, Lillford PJ, Hubbard RE (2001) Understanding the mechanism of ice binding by type III antifreeze proteins. J Mol Biol 305:875–889. doi:10.1006/jmbi.2000.4336
Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe—a multidimensional spectral processing system based on unix pipes. J Biomol NMR 6:277–293. doi:10.1007/BF00197809
Fletcher GL, Hew CL, Davies PL (2001) Antifreeze proteins from teleost fishes. Ann Rev Physiol 63:327–357. doi:10.1146/annurev.physiol.63.1.359
Garnham CP, Natarajan A, Middleton AJ, Kuiper MJ, Braslavsky I, Davies PL (2010) Compound ice-binding site of an antifreeze protein revealed by mutagenesis and fluorescent tagging. Biochemistry 49:9063–9071. doi:10.1021/bi100516e
Garnham CP, Campbell RL, Davies PL (2011) Anchored clathrate waters bind antifreeze proteins to ice. Proc Natl Acad Sci USA 108:7363–7367. doi:10.1073/pnas.1100429108
Garnham CP, Nishimiya Y, Tsuda S, Davies PL (2012) Engineering a naturally inactive isoform of type III antifreeze protein into one that can stop the growth of ice. FEBS Lett 586:3876–3881. doi:10.1016/j.febslet.2012.09.017
Goddard TD, Kneller DG (1997) SPARKY 3, University of California, San Francisco http://www.cgl.ucsf.edu/home/sparky/
Graether SP, Sykes BD (2004) Cold survival in freeze-intolerant insects: the structure and function of β-helical antifreeze proteins. Eur J Biochem 271:3285–3296. doi:10.1111/j.1432-1033.2004.04256.x
Graether SP, DeLuca CI, Baardsnes J, Hill GA, Davies PL, Jia Z (1999) Quantitative and qualitative analysis of type III antifreeze protein structure and function. J Biol Chem 274:11842–11847. doi:10.1074/jbc.274.17.11842
Güntert P (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278:353–378. doi:10.1385/1-59259-809-9:353
Howard EI, Blakeley MP, Haertlein M, Petit-Haertlein I, Mitschler A, Fisher SJ, Cousido-Siah A, Salvay AG, Popov A, Muller-Dieckmann C, Petrova T, Podjarny A (2011) Neutron structure of type-III antifreeze protein allows the reconstruction of AFP-ice interface. J Mol Recognit 24:724–732. doi:10.1002/jmr.1130
Kondo H, Hanada Y, Sugimoto H, Hoshino T, Garnham CP, Davies PL, Tsuda S (2012) Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation. Proc Natl Acad Sci 109:9360–9365. doi:10.1073/pnas.1121607109
Liou YC, Tociij A, Davies PL, Jia Z (2000) Mimicry of ice structure by surface hydroxyls and water of a β-helix antifreeze protein. Nature 406:322–324. doi:10.1038/35018604
Miura K, Ohgiya S, Hoshino T, Nemoto N, Suetake T, Miura A, Spyracopoulos L, Kondo H, Tsuda S (2001) NMR Analysis of Type III Antifreeze Protein Intramolecular Dimer. Structural basis for enhanced activity. J Biol Chem 276:1304–1310. doi:10.1074/jbc.M007902200
Nishimiya Y, Sato R, Takamichi M, Miura A, Tsuda S (2005) Co-operative effect of the isoforms of type III antifreeze protein expressed in Notched-fin eelpout, Zoarces elongatus Kner. FEBS J 272:482–492. doi:10.1111/j.1742-4658.2004.04490.x
Schwarzinger S, Kroon GJA, Foss TR, Wright PE, Dyson HJ (2000) Random coil chemical shifts in acidic 8 M urea: implementation of random coil shift data in NMRView. J Biomol NMR 18:43–48. doi:10.1023/A:1008386816521
Shen Y, Delaglio F, Cornilescu G, Bax A (2009) TALOS+: a hybrid method for predicting protein torsion angle from NMR chemical shifts. J Biomol NMR 44:213–223. doi:10.1007/s10858-009-9333-z
Sönnichsen FD, DeLuca CI, Davies PL, Sykes BD (1996) Refined solution structure of type III antifreeze protein: hydrophobic groups may be involved the energetics of the protein-ice interaction. Structure 4:1325–1337. doi:10.1016/S0969-2126(96)00140-2
Takamichi M, Nishimiya Y, Miura A, Tsuda S (2008) Fully active QAE isoform confers thermal hysteresis activity on a defective SP isoform of type III antifreeze protein. FEBS J 276:1471–1479. doi:10.1111/j.1742-4658.2009.06887.x
Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, Oldfield E, Markley JL, Sykes BD (1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6:135–140. doi:10.1007/BF00211777
Acknowledgments
The authors thank Prof. Peter Davies at Queen’s University for stimulating suggestions. This work was supported by a Grant-in-Aid for scientific research from the Japan Society for the Promotion of Science (JSPS) (No. 23310171) and from the Japan Bio-oriented Technology Research Advancement Institution (BRAIN).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kumeta, H., Ogura, K., Nishimiya, Y. et al. NMR structure note: a defective isoform and its activity-improved variant of a type III antifreeze protein from Zoarces elongates Kner . J Biomol NMR 55, 225–230 (2013). https://doi.org/10.1007/s10858-012-9703-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10858-012-9703-9