Determining the ice-binding planes of antifreeze proteins by fluorescence-based ice plane affinity

Journal of Visualized Experiments

Volumn , Issue 83, 2014, Pages

  Basu, Koli ^a   Garnham, Christopher P ^b   Nishimiya, Yoshiyuki ^c   Tsuda, Sakae ^c   Braslavsky, Ido ^d   Davies, Peter ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c National Institute of Advanced Industrial Science and Technology   (United States)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Antifreeze proteins; Chemistry; Fluorescent labeling; Ice adsorption; Ice lattice planes; Ice binding proteins; Issue 83; Life sciences; Materials; Optics; Single ice crystal

Indexed keywords

ANTIFREEZE PROTEIN; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; ICE; ISOPROTEIN;

ARTICLE; CHEMISTRY; CRYSTALLIZATION;

ANTIFREEZE PROTEINS; CRYSTALLIZATION; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; ICE; PROTEIN ISOFORMS;

EID: 84907637692     PISSN: 1940087X     EISSN: None     Source Type: Journal    
DOI: 10.3791/51185     Document Type: Article

References (35)

1. Devries, A.L. Antifreeze peptides and glycopeptides in cold-water fishes. Annu. Rev. Physiol. 45, 245-60 (1983).
2. Sidebottom, C., et al. Phytochemistry-heat-stable antifreeze protein from grass. Nature. 406 (6793), 256-256 (2000).
3. Tomczak, M.M., et al. A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophys. J. 82 (2), 874-81 (2002).
4. Gilbert, J.A., Davies, P.L., and Laybourn-Parry, J.A. Hyperactive, Ca2+-dependent antifreeze protein in an antarctic bacterium. FEMS Microbiol. Lett. 245(1), 67-72 (2005).
5. Garnham, C.P., Campbell, R.L., and Davies, P.L. Anchored clathrate waters bind antifreeze proteins to ice. Proc. Natl. Acad. Sci. U.S.A. 108 (18), 7363-7367 (2011).
6. Guo, S., Garnham, C.P., Whitney, J.C., Graham, L.A., and Davies, P.L. Re-evaluation of a bacterial antifreeze protein as an adhesin with ice-binding activity. Plos One. 7 (11), e48805 (2012).
7. Raymond, J.A. Algal ice-binding proteins change the structure of sea ice. Proc. Natl. Acad. Sci. U.S.A. 108 (24), E198-E198 (2011).
8. Raymond, J.A. and Devries, A.L. Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc. Natl. Acad. Sci. U.S.A. 74 (6), 2589-2593 (1977).
9. Baardsnes, J., et al. New ice-binding face for type i antifreeze protein. FEBS Lett. 463 (1-2), 87-91 (1999).
10. Middleton, A.J., Brown, A.M., Davies, P.L., and Walker, V.K. Identification of the ice-binding face of a plant antifreeze protein. FEBS Lett. 583 (4), 815-819 (2009).
11. Garnham, C.P., et al. Compound ice-binding site of an antifreeze protein revealed by mutagenesis and fluorescent tagging. Biochemistry. 49 (42), 9063-9071 (2010).
12. Nutt, D.R. and Smith, J.C. Dual function of the hydration layer around an antifreeze protein revealed by atomistic molecular dynamics simulations. J. Am. Chem. Soc. 130 (39), 13066-73 (2008).
13. Knight, C.A., Cheng, C.C., and Devries, A.L. Adsorption of alpha-helical antifreeze peptides on specific ice crystal-surface planes. Biophys. J. 59 (2), 409-418 (1991).
14. Antson, A.A., et al. Understanding the mechanism of ice binding by type iii antifreeze proteins. J. Mol. Biol. 305 (4), 875-89 (2001).
15. Graether, S.P., et al. Beta-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature. 406 (6793), 325-328 (2000).
16. Pertaya, N., Marshall, C.B., Celik, Y., Davies, P.L., and Braslavsky, I. Direct visualization of spruce budworm antifreeze protein interacting with ice crystals: Basal plane affinity confers hyperactivity. Biophys. J. 95 (1), 333-341 (2008).
17. Middleton, A.J., et al. Antifreeze protein from freeze-tolerant grass has a beta-roll fold with an irregularly structured ice-binding site. J. Mol. Biol. 416 (5), 713-724 (2012).
18. Scotter, A.J., et al. The basis for hyperactivity of antifreeze proteins. Cryobiology. 53 (2), 229-239 (2006).
19. Knight, C.A., Wierzbicki, A., Laursen, R.A., and Zhang, W. Adsorption of biomolecules to ice and their effects upon ice growth. 1. Measuring adsorption orientations and initial results. Crys. Growth Des. 1 (6), 429-438 (2001).
20. Hakim, A., et al. Crystal structure of an insect antifreeze protein and its implications for ice binding. J. Biol. Chem. 288 (17), 12295-304 (2013).
21. Garnham, C.P., Nishimiya, Y., Tsuda, S., and Davies, P.L. Engineering a naturally inactive isoform of type iii antifreeze protein into one that can stop the growth of ice. FEBS Lett. 586 (21), 3876-3881 (2012).
22. Holt, C.B. The effect of antifreeze proteins and poly(vinyl alcohol) on the nucleation of ice: A preliminary study. Cryo Letters. 24 (5), 323-30 (2003).
23. Knight, C.A. A simple technique for growing large, optically "perfect" ice crystals. J. Glac. 42 (142), 585-587 (1996).
24. Hobbs, P.V., Ice physics. Oxford: Clarendon Press. 200-248 (1974).
25. Knight, C. Formation of crystallographic etch pits on ice, and its application to the study of hailstones. J. Appl. Meteorol. 5 (5), 710-714 (1966).
26. Yang, D.S., Sax, M., Chakrabartty, A., and Hew, C.L. Crystal structure of an antifreeze polypeptide and its mechanistic implications. Nature. 333 (6170), 232-7 (1988).
27. Sicheri, F. and Yang, D.S. Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature. 375 (6530), 427-31 (1995).
28. Devries, A.L. Role of glycopeptides and peptides in inhibition of crystallization of water in polar fishes. Philos. T Roy. Soc. B. 304 (1121), 575-588 (1984).
29. Pertaya, N., et al. Fluorescence microscopy evidence for quasi-permanent attachment of antifreeze proteins to ice surfaces. Biophys. J. 92 (10), 3663-3673 (2007).
30. Kondo, H., et al. Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation. Proc. Natl. Acad. Sci. U.S.A. 109 (24), 9360-9365 (2012).
31. Mok, Y.F., et al. Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry. 49 (11), 2593-2603 (2010).
32. Takamichi, M., Nishimiya, Y., Miura, A., and Tsuda, S. Fully active qae isoform confers thermal hysteresis activity on a defective sp isoform of type iii antifreeze protein. FEBS J. 276 (5), 1471-1479 (2009).
33. Bar-Dolev, M., Celik, Y., Wettlaufer, J.S., Davies, P.L., and Braslavsky, I. New insights into ice growth and melting modifications by antifreeze proteins. J. R. Soc. Interface. 9 (77), 3249-3259 (2012).
34. Celik, Y., et al. Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth. Proc. Natl. Acad. Sci. U.S.A.110 (4), 1309-1314 (2013).
35. Garnham, C.P., Campbell, R.L., Walker, V.K., and Davies, P.L. Novel dimeric beta-helical model of an ice nucleation protein with bridged active sites. BMC Struct. Biol. 11, (2011).