Investigation of changes in structure and thermodynamic of spruce budworm antifreeze protein under subfreezing temperature

Nguyen, D. T., Colvin, M. E., Yeh, Y., Feeney, R. E. & Fink, W. H. The dynamics, structure, and conformational free energy of proline-containing antifreeze glycoprotein. Biophys. J. 82, 2892–2905 (2002). Yeh, Y. & Feeney, R. E. Antifreeze protein: Structure and mechanisms of function. Chem. Rev. 96, 601–618 (1996). Nguyen, H., Le, L. & Ho, T. B. Computational study on ice growth inhibition of Antarctic bacterium antifreeze protein using coarse grained simulation. J. Chem. Phys. 140, 225101 (2014). Raymond, J. A. Algal ice-binding proteins change the structure of sea ice. Proc. Natl. Acad. Sci. USA 108, E198 (2011). Janech, M. G., Krell, A., Mock, T., Kang, J. S. & Raymond, J. A. Ice-binding proteins from sea ice diatoms (Bacillariophyceae). J. Phycol. 42, 410–416 (2006). DeVries, A. L., Komatsu, S. K. & Feeney, R. E. Chemical and physical properties of freezing point depressing glycoproteins from Antarctic fishes. J. Biol. Chem. 245, 2901–2908 (1970). Davies, P. L., Hew, C. L. & Fletcher, G. L. Fish antifreeze proteins: physiology and evolutionary biology. Can. J. Zool. 66, 2611–2617 (1980). Marshall, C. B., Fletcher, G. L. & Davies, P. L. Hyperactive antifreeze protein in a fish. Nature 429, 153 (2004). Worrall, D. et al. A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 282, 115–117 (1998). Atici, O. & Nalbantoglu, B. Antifreeze proteins in higher plants. Phytochemistry 64, 1187–1196 (2003). Griffith, M. & Yaish, M. W. F. Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci. 9, 399–405 (2004). Tomchaney, A. P., Morris, J. P., Kang, S. H. & Duman, J. G. Purification, composition, and physical properties of thermal hysteresis “antifreeze” protein from larvae of the beetle, Tenebrio molitor. Biochemistry 21, 716–721 (1982). Hew, C. L., Kao, M. H., So, Y.-P. & Lim, K.-P. Presence of cystine-containing antifreeze proteins in the spruce budworm, Choristoneura fumiferana. Can. J. Zool. 61, 2324–2328 (1983). Schneppenheim, R. & Theede, H. Isolation and characterization of freezing-point depressing peptides from larvae of Tenebrio molitor. Comp. Biochem. Physol. 67, 561–568 (1980). Duman, J. G., Bennett, V., Sformo, T., Hochstrasser, R. & Barnes, B. M. Antifreeze proteins in Alaskan insects and spiders. J. Insect Physiol. 50, 259–266 (2004). Robinson, C. H. Cold adaptation in Arctic and Antarctic fungi. New Phytol. 151, 341–353 (2001). Gilbert, J. A., Hill, P. J., Dodd, C. E. & Laybourn-Parry . Demonstration of antifreeze protein activity in Antarctic lake bacteria. Microbiology 150, 171–180 (2004). Muryoi, N. et al. Antifreeze proteins: structures and mechanisms of function. Chem. Rev. 96, 601–618 (1996). Yeliz, C. et al. Microfluidic experiments reveal that antifreeze proteins bound to ice crystal suffice to prevent their growth. Proc. Natl. Acad. Sci. USA 110, 1309–1314 (2013). DeVries, A. L., Komatsu, S. K. & Feeney, R. E. Chemical and physical properties of freezing point-depressing glycoprotein from Antarctic fishes. J. Biol. Chem. 245, 2901–2908 (1970). Duman, J. G. Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu. Rev. Physiol. 63, 327–357 (2001). Walters, K. R. Jr. et al. A thermal hysteresis-producing xylomannan glycolipid antifreeze associated with cold tolerance is found in diverse taxa. J. Comp. Physiol. B 181, 631–640 (2011). Meister, K. et al. Observation of ice-like water layers at an aqueous protein surface. Proc. Natl. Acad. Sci. USA 111, 17732–17736 (2014). Duboué-Dijon, E. & Laage, D. Comparative study of hydration shell dynamics around a hyperactive antifreeze protein and around ubiquitin. J. Chem. Phys. 141, 22D529 (2014). Jorov, A., Zhorov, B. S. & Yang, D. S. Theoretical Study of interaction of winter flounder antifreeze protein with ice. Protein Sci. 13, 1524–1537 (2004). Drori, R., Celik, Y., Davies, P. L. & Braslavsky, I. Ice-binding proteins that accumulate on different ice crystal planes produce distinct thermal hysteresis dynamics. J. R. Soc. Interface 11, 20140526 (2014). John, G. D. & Olsen, T. M. Thermal hysteresis protein activity in bacteria, fungi and phylogenetically diverse plants. Cryobiology 30, 322–328 (1993). Fletcher, G. L., Hew, C. L. & Davies, P. L. Antifreeze proteins of teleost fishes. Annu. Rev. Physiol. 63, 359–390 (2001). Nguyen, H., Van, T. D. & Le, L. Coarse grained simulation reveals antifreeze properties of hyperactive antifreeze protein from Antarctic bacterium Colwellia sp. Chem. Phys. Lett. 638, 137–143 (2015). Nguyen, H., Van, T. D., Tran, N. & Le, L. Exploring the effects of subfreezing temperature and salt concentration on ice growth inhibition of Antarctic Gram-Negative bacterium Marinomonas Promoryensis using coarse-grained simulation. Appl. Biochem. Biotechnol. 178, 1534–1545 (2016). Rajiv, K. K. & Anirban, B. Will it be beneficial to simulate the antifreeze proteins at ice freezing condition or at lower temperature? J. Phys. Chem. B 119, 11485–11495 (2015). Garnham, C. P., Campbell, R. L. & Davies, P. L. Anchored clathrate waters bind antifreeze proteins to ice. Proc. Natl. Acad. Sci. USA 108, 7363–7367 (2011). Davies, P. L., Baardsnes, J., Kuiper, M. J. & Walker, V. K. Structure and function of antifreeze proteins. Philos. Trans R Soc. Lond. B Biol. Sci. 357, 927–935 (2002). Devries, A. L. & Lin, Y. Structure of a peptide antifreeze and mechanism of adsorption to ice. Biochim. Biophys. Acta. 495, 388–392 (1977). Chao, H. et al. A diminished role for hydrogen bonds in antifreeze protein binding to ice. Biochemistry 36, 14652–14660 (1997). Baardsnes, J. et al. New ice-binding face for type I antifreeze protein. FEBS Lett. 463, 87–91 (1999). Nutt, D. R. & Smith, J. C. Dual function of the hydration layer around an antifreeze protein revealed by atomistic molecular dynamics simulations. J. Am. Chem. Soc. 130, 13066–13073 (2008). Midya, U. S. & Bandyopadyay, S. Hydration behavior at the ice-binding surface of the Tenebrio molitor antifreeze protein. J. Phys. Chem. B 118, 4743–4752 (2014). Gallagher, K. R. & Sharp, K. A. Analysis of thermal hysteresis protein hydration using the random network model. Biophys. Chem. 105, 195–209 (2003). Smolin, N. & Daggett, V. Formation of ice-like water structure on the surface of an antifreeze protein. J. Phys. Chem. B 112, 6193–6202 (2008). Wierzbicki, A. et al. Antifreeze proteins at the ice/water interface: Three calculated discriminating properties for orientation of type I proteins. Biophys. J. 93, 1442–1451 (2007). Yang, C. & Sharp, K. A. The mechanism of the type III antifreeze protein action: A computational study. Biophys. Chem. 109, 137–148 (2004). Yang, C. & Sharp, K. A. Hydrophobic tendency of polar group hydration as a major force in type I antifreeze protein recognition. Proteins 59, 266–274 (2005). Jinhong, W. et al. Isolation and characterization of secricin antifreeze peptides and molecular dynamics modelling of their ice-binding interaction. Food Chem. 23, 621–629 (2015). Kuiper, M. J., Morton, C. J., Abraham, S. E. & Gray-Weale, A. The biological function of an insect antifreeze protein simulated by molecular dynamics. eLife 4, e05142 (2015). Bar, M., Celik, Y., Fass, D. & Braslavsky, I. Interactions of β-Helical Antifreeze Protein Mutants with Ice. Cryst. Growth Des. 8, 2954–2963 (2008). Steffen, P. G. et al. Spruce budworm antifreeze protein: Changes in structure and dynamics at low temperature. J. Mol. Biol. 327, 1155–1168 (2003). Humphrey, W., Dalke, A. & Schulten, K. VMD-visual molecular dynamics. Molecular Graphics 14, 33–38 (1996). Kar, R. K. & Bhunia, A. Biophysical and Biochemical Aspects of Antifreeze Proteins: Using Computational Tools to Extract Atomistic Information. Prog. Biophys. Mol. Biol. 119, 194–204 (2015). Sanz, E., Vega, C., Abascal, J. L. F. & MacDowell, L. G. Phase diagram of water from computer simulation. Phys. Rev. Lett. 92, 255701 (2004). Kofke, D. A. & Post, A. J. Hard particles in narrow pores. Transfer-matrix solution and the periodic narrow box. J. Chem. Phys. 98, 1331–1336 (1993). Frisch, M. J. et al. Gaussian 03, revision C.02, Gaussian, Inc.: Wallingford, CT (2004). Justin, A. L., William, J. A. & David, R. B. Practical considerations for building GROMOS-Compatible small-Molecule topologies. J. Chem. Inf. Model. 50, 2221–2235 (2010). Schüttelkopf, A. W. & van Aalten, D. M. PRODRG: a tool for high-thoughput crystallography of protein-ligand complexes. Acta Crystalloqr. D Biol. Crystalloqr. 60, 1355–1363 (2004). Gunsteren, W. F. van . et al. Biomolecular Simulation: The GROMOS96 manual and userguide. Vdf Hochschulverlag AG an der ETH Zurich, Zurich, Switzerland. 1–1042 (1996). Hess, B., Kutzner, C., Spoel, Dvd & Lindahl, E. GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Inf. Model. 4, 435–447 (2008). Mark, P. & Nilsson, L. Structure and Dynamics of the TIP3P, SPC, and SPC/E Water Models at 298 K. J. Phys. Chem. A 105, 9954–9960 (2001). Hess, B., Bekker, H., Berendsen, H. J. C. & Fraaije, J. G. E. M. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463–1472 (1997). Darden, T., York, D. & Pedersen, L. Particle mesh Ewald: An N-log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089–10092 (1993). Berendsen, H. J. C., Postma, J. P. M., Gunsteren, W. F. van, DiNola, A. & Haak, L. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684–3690 (1984). Parrinello, M. & Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys. 52, 7182–7190 (1981). Hockney, R. W., Goel, S. P. & Eastwood, J. W. Quit high-resolution computer models of plasma. J. Comp. Phys. 14, 148–158 (1974). Lamb, D. & Verlinde, H. Vapor-growth of individual ice crystal. Physics and Chemistry of Clouds. Cambridge University Press, Ch 8.3, 342–369 (2011).