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Proteins in amorphous saccharide matrices: Structural and dynamical insights on bioprotection

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Abstract

Bioprotection by sugars, and in particular trehalose peculiarity, is a relevant topic due to the implications in several fields. The underlying mechanisms are not yet clearly elucidated, and remain the focus of current investigations. Here we revisit data obtained at our lab on binary sugar/water and ternary protein/sugar/water systems, in wide ranges of water content and temperature, in the light of the current literature. The data here discussed come from complementary techniques (Infrared Spectroscopy, Molecular Dynamics simulations, Small Angle X-ray Scattering and Calorimetry), which provided a consistent description of the bioprotection by sugars from the atomistic to the macroscopic level. We present a picture, which suggests that protein bioprotection can be explained in terms of a strong coupling of the biomolecule surface to the matrix via extended hydrogen-bond networks, whose properties are defined by all components of the systems, and are strongly dependent on water content. Furthermore, the data show how carbohydrates having similar hydrogen-bonding capabilities exhibit different efficiency in preserving biostructures.

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References

  1. L.M. Crowe, Comp. Biochem. Physiol. A 132, 505 (2002).

    Article  Google Scholar 

  2. J.H. Crowe, Adv. Exp. Med. Biol. 594, 143 (2007).

    Article  Google Scholar 

  3. J. Green, C.A. Angell, J. Phys. Chem. 93, 2880 (1989).

    Article  Google Scholar 

  4. J.F. Carpenter, J.H. Crowe, Biochemistry 28, 3916 (1989).

    Article  Google Scholar 

  5. P.S. Belton, A.M. Gil, Biopolymers 34, 957 (1994).

    Article  Google Scholar 

  6. S.N. Timasheff, Biochemistry 41, 13473 (2002).

    Article  Google Scholar 

  7. J.G. Sampedro, S. Uribe, Mol. Cell Biochem. 256, 319 (2004).

    Article  Google Scholar 

  8. S.D. Allison, B. Chang, T.W. Randolph, J.F. Carpenter, Arch. Biochem. Biophys. 365, 289 (1999).

    Article  Google Scholar 

  9. W.F. Wolkers, H. Oldenhof, M. Alberda, F.A. Hoekstra, Biochim. Biophys. Acta-Gen. Subj. 1379, 83 (1998).

    Article  Google Scholar 

  10. S.H. Gaffney, E. Haslam, T.H. Lilley, T.R.J. Ward, J. Chem. Soc. Faraday Trans. 84, 2545 (1998).

    Article  Google Scholar 

  11. F. Sussich, C. Skopec, J. Brady, A. Cesàro, Carbohydr. Res. 334, 165 (2001).

    Article  Google Scholar 

  12. C. Branca, S. Magazù, G. Maisano, P. Migliardo, J. Chem. Phys. 11, 281 (1999).

    Article  ADS  Google Scholar 

  13. S. Magazù, G. Maisano, F. Migliardo, C. Mondelli, Biophys. J. 86, 3241 (2004).

    Article  ADS  Google Scholar 

  14. A. Hédoux, J.-F. Willart, R. Ionov, F. Affouard Y. Guinet, L. Paccou, A. Lerbret, M. Descamps, J. Phys. Chem. B 110, 22886 (2006).

    Article  Google Scholar 

  15. J.-A. Seo, A. Hédoux, Y. Guinet, L. Paccou, F. Affouard, A. Lerbret, M. Descamps, J. Phys. Chem. B 114, 6675 (2010).

    Article  Google Scholar 

  16. A. Lerbret, F. Affouard, P. Bordat, A. Hedoux, Y. Guinet, M. Descamps, J. Chem. Phys. 24, 245103 (2009).

    Article  ADS  Google Scholar 

  17. A. Hédoux, F. Affouard, M. Descamps, Y. Guinet, L. Paccou, J. Phys.: Condens. Matter 19, 205142 (2007).

    Article  ADS  Google Scholar 

  18. A. Hédoux, J.F. Willart, L. Paccou, Y. Guinet, F. Affouard, A. Lerbret, M. Descamps, J. Phys. Chem. B 113, 6119 (2009).

    Article  Google Scholar 

  19. A. Lerbret, F. Affouard, P. Bordat, A. Hédoux, Y. Guinet, M. Descamps, J. Non-Cryst. Solids 357, 695 (2011).

    Article  ADS  Google Scholar 

  20. L. Cordone, M. Ferrand, E. Vitrano, G. Zaccai, Biophys. J. 76, 1043 (1999).

    Article  Google Scholar 

  21. L. Cordone, G. Cottone, S. Giuffrida, G. Palazzo, G. Venturoli, C. Viappiani, BBA-Proteins Proteomics 1749, 252 (2005) and references therein.

    Article  Google Scholar 

  22. L. Cordone, G. Cottone, S. Giuffrida, J. Phys.: Condens. Matter 19, 205110 (2007) and references therein.

    Article  ADS  Google Scholar 

  23. A. Lerbret, F. Affouard, A. Hédoux, S. Krenzlin, J. Siepmann, M.C. Bellissent-Funel, M. Descamps, J. Phys. Chem. B 116, 11103 (2012).

    Article  Google Scholar 

  24. F. Francia, M. Dezi, A. Mallardi, G. Palazzo, L. Cordone, G. Venturoli, J. Am. Chem. Soc. 130, 10240 (2008).

    Article  Google Scholar 

  25. M.V. Fedorov, J.M. Goodman, D. Nerukh, S. Schumm, Phys. Chem. Chem. Phys. 13, 2294 (2011).

    Article  Google Scholar 

  26. S. Giuffrida, G. Cottone, F. Librizzi, L. Cordone, J. Phys. Chem. B 107, 13211 (2003).

    Article  Google Scholar 

  27. S. Giuffrida, G. Cottone, L. Cordone, J. Phys. Chem. B 108, 15415 (2004).

    Article  Google Scholar 

  28. S. Giuffrida, G. Cottone, L. Cordone, Biophys. J. 91, 968 (2006).

    Article  ADS  Google Scholar 

  29. H. Frauenfelder, F. Parak, R.D. Young, Annu. Rev. Biophys. Chem. 17, 451 (1988).

    Article  Google Scholar 

  30. J. Vojtechovský, K. Chu, J. Berendzen, R.M. Sweet, I. Schlichting, Biophys. J. 77, 2153 (1999).

    Article  Google Scholar 

  31. D. Eisenberg, W. Kauzmann, The Structure and Properties of Water (Oxford University Press, London, 1969).

  32. S. Giuffrida, G. Cottone, E. Vitrano, L. Cordone, J. Non-Cryst. Solids 357, 677 (2011).

    Article  ADS  Google Scholar 

  33. L. Cordone, G. Cottone, S. Giuffrida, F. Librizzi, Chem. Phys. 345, 275 (2008).

    Article  ADS  Google Scholar 

  34. U. Samuni, D. Dantsker, C.J. Roche, J.M. Friedman, GENE 398, 234 (2007) and references therein.

    Article  Google Scholar 

  35. A.M. Massari, I.J. Finkelstein, B.L. McClain, A. Goj, X. Wen, K.L. Bren, R.F. Loring, M.D. Fayer, J. Am. Chem. Soc. 127, 14279 (2005).

    Article  Google Scholar 

  36. M. Heyden, E. Bründermann, U. Heugen, G. Niehues, D.M. Leitner, M. Havenith, J. Am. Chem. Soc. 130, 5773 (2008).

    Article  Google Scholar 

  37. M. Paolantoni, L. Comez, M.E. Gallina, P. Sassi, F. Scarponi, D. Fioretto, A. Morresi, J. Phys. Chem. B 113, 7874 (2009).

    Article  Google Scholar 

  38. L. Lupi, L. Comez, M. Paolantoni, D. Fioretto, B.M. Ladanyi, J. Phys. Chem. B 116, 7499 (2012).

    Article  Google Scholar 

  39. S. Perticaroli, L. Comez, M. Paolantoni, P. Sassi, L. Lupi, D. Fioretto, A. Paciaroni, A. Morresi, J. Phys. Chem. B 114, 8262 (2010).

    Article  Google Scholar 

  40. D.P. Miller, J.J. de Pablo, J. Phys. Chem. B 104, 8876 (2000).

    Article  Google Scholar 

  41. G. Cottone, G. Ciccotti, L. Cordone, J. Chem. Phys. 117, 9862 (2002).

    Article  ADS  Google Scholar 

  42. G. Cottone, S. Giuffrida, G. Ciccotti, L. Cordone, Proteins 59, 291 (2005).

    Article  Google Scholar 

  43. G. Cottone, J. Phys. Chem. B 111, 3563 (2007).

    Article  Google Scholar 

  44. L. Maragliano, G. Cottone, L. Cordone, G. Ciccotti, Biophys. J. 86, 2765 (2004).

    Article  ADS  Google Scholar 

  45. D. Vitkup, D. Ringe, G.A. Petsko, M. Karplus, Nat. Struct. Biol. 7, 34 (2000).

    Article  Google Scholar 

  46. G. Cottone, L. Cordone, G. Ciccotti, Biophys. J. 80, 931 (2001).

    Article  ADS  Google Scholar 

  47. R.D. Lins, C.S. Pereira, P.H. Hunemberger, Proteins 55, 177 (2004).

    Article  Google Scholar 

  48. M. Tarek, D.J. Tobias, Phys. Rev. Lett. 88, 138101 (2002).

    Article  ADS  Google Scholar 

  49. M. Tarek, D.J. Tobias, Biophys. J. 79, 3244 (2000).

    Article  ADS  Google Scholar 

  50. A. Luzar, D. Chandler, Phys. Rev. Lett. 76, 928 (1996).

    Article  ADS  Google Scholar 

  51. E.C. Lopez-Diez, S. Bone, Phys. Med. Biol. 45, 3577 (2000).

    Article  Google Scholar 

  52. L. Giachini, F. Francia, L. Cordone, F. Boscherini, G. Venturoli, Biophys. J. 92, 1350 (2007).

    Article  ADS  Google Scholar 

  53. P.B. Conrad, J.J. de Pablo, J. Phys. Chem. A 103, 4049 (1999).

    Article  Google Scholar 

  54. A. Longo, S. Giuffrida, G. Cottone, L. Cordone, Phys. Chem. Chem. Phys. 12, 6852 (2010).

    Article  Google Scholar 

  55. S. Giuffrida, M. Panzica, F.M. Giordano, A. Longo, Eur. Phys. J. E 34, 87 (2011).

    Article  Google Scholar 

  56. G.M. Brown, H.A. Levy, Acta Cryst. B 29, 790 (1973).

    Article  Google Scholar 

  57. K. Ibel, H.B. Stuhrmann, J. Mol. Biol. 93, 255 (1975).

    Article  Google Scholar 

  58. J.S. Pedersen, Adv. Colloid Interface Sci. 70, 171 (1997).

    Article  Google Scholar 

  59. A. Lerbret, P. Bordat, F. Affouard, M. Descamps, F. Migliardo, J. Phys. Chem. 109, 11046 (2005).

    Google Scholar 

  60. J.E. Curtis, H. Nanda, S. Khodadadi, M. Cicerone, H.J. Lee, A. McAuley, S. Krueger, J. Phys. Chem. B 116, 9653 (2012).

    Article  Google Scholar 

  61. F. Sussich, C.E. Skopec, J.W. Brady, A. Cesàro, Food Chem. 122, 388 (2010).

    Article  Google Scholar 

  62. F. Ledl, E. Schleicher, Angew. Chem., Int. Ed. 29, 565 (1990).

    Article  Google Scholar 

  63. G. Bellavia, G. Cottone, S. Giuffrida, A. Cupane, L. Cordone, J. Phys. Chem. B 113, 11543 (2009).

    Article  Google Scholar 

  64. G. Bellavia, S. Giuffrida, G. Cottone, A. Cupane, L. Cordone, J. Phys. Chem. B 115, 6340 (2011).

    Article  Google Scholar 

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Correspondence to S. Giuffrida.

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Contribution to the Topical Issue “Neutron Biological Physics”, edited by Giovanna Fragneto and Frank Gabel.

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Giuffrida, S., Cottone, G., Bellavia, G. et al. Proteins in amorphous saccharide matrices: Structural and dynamical insights on bioprotection. Eur. Phys. J. E 36, 79 (2013). https://doi.org/10.1140/epje/i2013-13079-x

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