Interaction of the Disaccharide Trehalose with a Phospholipid Bilayer: A Molecular Dynamics Study

Biophysical Journal

Volumn 86, Issue 4, 2004, Pages 2273-2285

  Pereira, Cristina S ^a,b   Lins, Roberto D ^a   Chandrasekhar, Indira ^a   Freitas, Luiz Carlos G ^b   Hünenberger, Philippe H ^a  

^a ETH ZURICH   (Switzerland)

^b FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

DISACCHARIDE; PHOSPHOLIPID; TREHALOSE;

ARTICLE; HYDROGEN BOND; LIPID MEMBRANE; MOLECULAR DYNAMICS; PHOSPHOLIPID BILAYER; PROTEIN STRUCTURE; SIMULATION; STRESS; TEMPERATURE;

EID: 1942519438     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74285-X     Document Type: Article

References (86)

1. Ballone, P., M. Marchi, C. Branca, and S. Magazu. 2000. Structural and vibrational properties of trehalose: a density functional study. J. Phys. Chem. B. 104:6313-6317.
2. Behm, C. A. 1997. The role of trehalose in the physiology of nematodes. Int. J. Parasitol. 27:215-229.
3. Belton, P. S., and A. H. Gil. 1994. IR and Raman spectroscopic studies of the interaction of trehalose with hen egg white lysozyme. Biopolymers. 34:957-961.
4. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. DiNola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
5. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, and J. Hermans. 1981. Interaction models for water in relation to protein hydration. In Intermolecular Forces. B. Pullman, editor. Reidel, Dordrecht, The Netherlands. 331-342.
6. Birch, G. G. 1972. Mushroom sugar. In Health and Food. G. G. Birch, L. F. Green, and I. G. Plaskett, editors. Elsevier Science, New York. 49-53.
7. Branca, C., S. Magazu, G. Maisano, S. M. Bennington, and B. Fak. 2003. Vibrational studies on disaccharide/H2O systems by inelastic neutron scattering, Raman, and IR spectroscopy. J. Phys. Chem. B. 107:1444-1451.
8. Branca, C., S. Magazu, G. Maisano, and P. Migliardo. 1999. Anomalous cryoprotective effectiveness of trehalose: Raman scattering evidences. J. Chem. Phys. 111:281-287.
9. Bryant, G., and J. Wolfe. 1992. Interfacial forces in cryobiology and anhydrobiology. Cryo-Letters. 13:23-36.
10. Carpenter, J. F., S. J. Prestrelski, T. J. Anchordoguy, and T. Arakawa. 1994. Interactions of stabilizers with proteins during freezing and drying. In Formulation and Delivery of Proteins and Peptides. J. L. Cleland and R. Langer, editors. American Chemical Society, Washington, DC. 134-147.
11. Chandrasekhar, I., and B. P. Gaber. 1988. Stabilization of the biomembrane by small molecules: interaction of trehalose with the phospholipids bilayer. J. Biomol. Struct. Dyn. 5:1163-1171.
12. Chandrasekhar, I., M. Kastenholz, R. D. Lins, C. Oostenbrink, L. D. Schuler, D. P. Tieleman, and W. F. van Gunsteren. 2003. A consistent potential energy parameter set for lipids: dipalmitoylphosphatidylcholine as a benchmark of the GROMOS96 45A3 force field. Eur. Biophys. J. 32:67-77.
13. Clegg, J. S. 1965. The origin of trehalose and its significance during formation of encysted dormant embryos of Artemia salina. Comp. Biochem. Physiol. 14:135-143.
14. Clegg, J. S. 1997. Embryos of Artemia franciscana survive four years of continuous anoxia: the case for complete metabolic rate depression. J. Exp. Biol. 200:467-475.
15. Clegg, J. S. 2001. Cryptobiosis - a peculiar state of biological organization. Comp. Biochem. Physiol. 128B:613-624.
16. Clegg, J. S., and S. A. Jackson. 1992. Aerobic heat-shock activates trehalose synthesis in embryos of Anemia franciscana. FEBS Lett. 303:45-47.
17. Conrad, P. B., and J. J. de Pablo. 1999. Computer simulation of the cryoprotectant disaccharide alpha, alpha-trehalose in aqueous solution. J. Phys. Chem. A. 103:4049-4055.
18. Cottone, G., G. Ciccotti, and L. Cordone. 2002. Protein trehalose-water structures in trehalose coated carboxy-myoglobin. J. Chem. Phys. 117: 9862-9866.
19. Cottone, G., L. Cordone, and G. Ciccotti. 2001. Molecular dynamics simulation of carboxy-myoglobin embedded in a trehalose-water matrix. Biophys. J. 80:931-938.
20. Crowe, L. M. 2002. Lessons from nature: the role of sugars in anhydrobiosis. Comp. Biochem. Physiol. 131A:505-513.
21. Crowe, J. H., J. F. Carpenter, and L. M. Crowe. 1998a. The role of vitrification in anhydrobiosis. Annu. Rev. Physiol. 60:73-103.
22. Crowe, J. H., J. S. Clegg, and L. M. Crowe. 1998b. Anhydrobiosis: the water replacement hypothesis. In The Properties of Water in Foods (ISO-POW 6). D. S. Reid, editor. Chapman and Hall, New York. 440-455.
23. Crowe, J. H., L. M. Crowe, J. F. Carpenter, S. Prestrelski, F. A. Hoekstra, P. de Araújo, and A. D. Panek. 1997. Anhydrobiosis: cellular adaptation to extreme dehydration. In Handbook of Physiology, Vol. 2. W. H. Dantzler, editor. Oxford University Press, Oxford, UK. 1445-1477.
24. Crowe, J. H., L. M. Crowe, J. F. Carpenter, and C. A. Wistrom. 1987. Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem. J. 242:1-10.
25. Crowe, J. H., L. M. Crowe, and D. Chapman. 1984. Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science. 223:701-703.
26. Crowe, J. H., L. M. Crowe, A. E. Oliver, N. Tsvetkova, W. Wolkers, and F. Tablin. 2001. The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state. Cryobiology. 43:89-105.
27. Crowe, J. H., F. A. Hoekstra, and L. M. Crowe. 1992. Anhydrobiosis. Annu. Rev. Physiol. 54:579-599.
28. Crowe, J. H., A. E. Oliver, and F. Tablin. 2002. Is there a single biochemical adaptation to anhydrobiosis? Integr. Comp. Biol. 42:497-503.
29. Crowe, J. H., F. Tablin, W. F. Wolkers, K. Gousset, N. M. Tsvetkova, and J. Ricker. 2003. Stabilization of membranes in human platelets freeze-dried with trehalose. Chem. Phys. Lipids. 122:41-52.
30. Damore, T. G., R. G. Crumplen, and G. G. Stewart. 1991. The involvement of trehalose in yeast stress tolerance. J. Ind. Microbiol. 7:191-195.
31. Douliez, J. P., A. Leonard, and E. J. Dufourc. 1995. Restatement of order parameters in biomembranes: calculation of C-C bond order parameters from C-D quadrupolar splittings. Biophys. J. 68:1727-1739.
32. Egberts, E., and H. J. C. Berendsen. 1988. Molecular dynamics simulation of a smectic liquid crystal with atomic detail. J. Chem. Phys. 89:3718-3732.
33. Ekdawi-Sever, N., J. J. de Pablo, E. Feick, and E. von Meerwall. 2003. Diffusion of sucrose and alpha, alpha-trehalose in aqueous solutions. J. Phys. Chem. A. 107:936-943.
34. Elbein, A. D., Y. T. Pan, I. Pastuszak, and D. Carrol. 2003. New insights on trehalose: a multifunctional molecule. Glycobiology. 13:17R-27R.
35. Eleutherio, E. C. A., J. T. Silva, and A. Panek. 1993. Role of the trehalose carrier in dehydration resistance of S. cervisiae. Biochim. Biophys. Acta. 1156:263-266.
36. Engelsen, S. B., and S. Perez. 2000. Unique similarity of the asymmetric trehalose solid-state hydration and the diluted aqueous-solution hydration. J. Phys. Chem. B. 104:9301-9311.
37. Eroglu, A., M. Toner, and T. L. Toth. 2002. Beneficial effect of microinjected trehalose on the cryosurvival of human oocytes. Fertil. Steril. 77:152-158.
38. Feofilova, E. P. 2003. Deceleration of vital activity as a universal biochemical mechanism ensuring adaptation of microorganisms to stress factors: a review. Appl. Biochem. Microbiol. 39:1-18.
39. Fukuse, T., T. Hirata, T. Nakamura, M. Ueda, M. Kawashima, S. Hitomi, and H. Wada. 1999. Role of saccharides on lung preservation. Transplantation. 68:110-117.
40. Guppy, M., and P. Withers. 1999. Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev. 74:1-40.
41. Hockney, R. W. 1970. The potential calculation and some applications. Methods Comput. Phys. 9:136-211.
42. Hoekstra, F. A., W. F. Wolkers, J. Buitink, E. A. Golovina, J. H. Crowe, and L. M. Crowe. 1997. Membrane stabilization in the dry state. Comp. Biochem. Physiol. 117A:335-341.
43. Keilin, D. 1959. The problem of anabiosis or latent life: history and current concept. Proc. R. Soc. Lond. B Biol. Sci. 150:149-191.
44. Koch, E. M., and F. C. Koch. 1925. The presence of trehalose in yeast. Science. 61:570-572.
45. Koster, K. L., Y. P. Lei, M. Anderson, S. Martin, and G. Bryant. 2000. Effects of vitrified and nonvitrified sugars on phosphatidylcholine fluid-to-gel phase transitions. Biophys. J. 78:1932-1946.
46. Koster, K. L., M. S. Webb, and G. Bryant. 1994. Interactions between soluble sugars and POPC (1-palmitoyl-2-oleoylphosphatidylcholine) during dehydration: vitrification of sugars alters the phase-behavior of the phospholipid. Biochim. Biophys. Acta. 1193:143-150.
47. Lambruschini, C., N. Relini, A. Ridi, L. Cordone, and A. Gliozzi. 2000. Trehalose interacts with phospholipid polar heads in Langmuir monolayers. Langmuir. 16:5467-5470.
48. Lee, C. W. B., J. S. Waugh, and R. G. Griffin. 1986. Solid-state NMR-study of trehalose/1,2-dipalmitoyl-sn-phosphatidylcholine interactions. Biochemistry. 25:3737-3742.
49. Lins, R. D., C. S. Pereira, and P. H. Hünenberger. 2004. Trehalose-protein interaction in aqueous solution. Proteins. 55:177-186.
50. Liu, Q., R. K. Schmidt, B. Teo, P. A. Karplus, and J. W. Brady. 1997. Molecular dynamics studies of the hydration of alpha, alpha-trehalose. J. Am. Chem. Soc. 119:7851-7862.
51. Luzardo, M. D., F. Amalfa, A. M. Nunez, S. Diaz, A. C. B. de Lopez, and E. A. Disalvo. 2000. Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys. J. 78:2452-2458.
52. Madin, K. A. C., and J. Crowe. 1975. Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during drying. J. Exp. Zool. 193:335-342.
53. Matsuo, T. 2001. Trehalose protects comeal epithelial cells from death by drying. Br. J. Ophthalmol. 85:610-612.
54. Matsuo, T., Y. Tsuchida, and N. Morimoto. 2002. Trehalose eye drops in the treatment of dry eye syndrome. Ophthalmology. 109:2024-2029.
55. Nagase, H., H. Ueda, and M. Nakagaki. 1999. Relationship between hydrophobic index of saccharide and gel-liquid crystal transition temperature of the L-alpha-dipalmitoyl phosphatidylcholine (DPPC)/saccharide/water system. Chem. Pharm. Bull. 47:607-610.
56. Nagle, J. F., and S. Tristram-Nagle. 2000. Structure of lipid bilayers. Biochim. Biophys. Acta. 1469:159-195.
57. Nakagaki, M., H. Nagase, and H. Ueda. 1992. Stabilization of the lamellar structure of phosphatidylcholine by complex-formation with trehalose. J. Membr. Sci. 73:173-180.
58. Norcia, M. A. 2000. Compositions and methods for wound management. Off. Gaz. Pat. Office, 1232:424-448.
59. Oliver, A. E., O. Leprince, W. F. Wolkers, D. K. Hincha, A. G. Heyer, and J. H. Crowe. 2001. Non-disaccharide-based mechanisms of protection during drying. Cryobiology. 43:151-167.
60. Richards, A. B., S. Krakowka, L. B. Dexter, H. Schmid, A. P. M. Wolterbeek, D. H. Waalkens-Berendsen, A. Shigoyuki, and M. Kurimoto. 2002. Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem. Toxicol. 40:871-898.
61. Ricker, J. V., N. M. Tsvetkova, W. F. Wolkers, C. Leidy, F. Tablin, M. Longo, and J. H. Crowe. 2003. Trehalose maintains phase separation in an air-dried binary lipid mixture. Biophys. J. 84:3045-3051.
62. Rudolph, B. R., I. Chandrasekhar, B. P. Gaber, and M. Nagumo. 1990. Molecular modeling of saccharide-lipid Interactions. Chem. Phys. Lipids. 53:243-261.
63. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of cartesian equations of motion of a system with constraints molecular dynamics of n-alkanes. J. Comput. Phys. 23:327-341.
64. Sackmann, E. 1995. Physical basis of self-organization and function of membranes: physics of vesicles. In Handbook of Biological Physics, Vol. 1A, Structure and Dynamics of Membranes. R. Lipowsky and E. Sackman, editors. Elsevier, Amsterdam, The Netherlands. 213-304.
65. Schuler, L. D., X. Daura, and W. F. van Gunsteren. 2001. An improved GROMOS96 force field for aliphatic hydrocarbons in the condensed phase. J. Comput. Chem. 22:1205-1218.
66. Scott, P. 2000. Resurrection plants and the secrets of the leaf. Ann. Bot. 85:159-166.
67. Singer, M. A., and S. Lindquist. 1998. Thermotolerance in Saccharomyces cerevisiae: the yin and yang of trehalose. Trends Biotechnol. 16:460-468.
68. Somme, L. 1996. Anhydrobiosis and cold tolerance in tardigrades. Eur. J. Entomol. 93:349-357.
69. Sun, W. Q., T. C. Irving, and A. C. Leopold. 1994. The role of sugar, vitrification and membrane phase-transition in seed desiccation tolerance. Physiol. Plantarum. 90:621-628.
70. Sun, W. Q., and A. C. Leopold. 1994. Glassy state and seed storage stability: a viability equation analysis. Ann. Bot. 74:601-604.
71. Sun, W. Q., and A. C. Leopold. 1997. Cytoplasmic vitrification acid survival of anhydrobiotic organisms. Comp. Biochem. Physiol. 117A: 327-333.
72. Sun, W. Q., A. C. Leopold, L. M. Crowe, and J. H. Crowe. 1996. Stability of dry liposomes in sugar glasses. Biophys. J. 70:1769-1776.
73. Sussich, F., C. Skopec, J. Brady, and A. Cesaro. 2001. Reversible dehydration of trehalose and anhydrobiosis: from solution state to an exotic crystal? Carbohydr. Res. 334:165-176.
74. Takahashi, H., H. Ohmae, and I. Hatta. 1997. Trehalose-induced destabilization of interdigitated gel phase in dihexadecylphosphatidylcholine. Biophys. J. 73:3030-3038.
75. Timasheff, S. N. 1982. The control of protein stability and association by weak-interactions with water. In Biophysics of Water. F. Franks and S. Mathias, editors. Wiley, New York. 70-72.
76. Tironi, I. G., R. Sperb, P. E. Smith, and W. F. van Gunsteren. 1995. A generalized reaction field method for molecular dynamics simulations. J. Chem. Phys. 102:5451-5459.
77. Tsvetkova, N. M., B. L. Phillips, L. M. Crowe, J. H. Crowe, and S. H. Risbud. 1998. Effect of sugars on headgroup mobility in freeze-dried dipalmitoylphosphatidylcholine bilayers: solid-state P-31 NMR and FTIR studies. Biophys. J. 75:2947-2955.
78. van Gunsteren, W. F., and H. J. C. Berendsen. 1990. Computer simulation of molecular dynamics: methodology, applications and perspectives in chemistry. Angew. Chem. Int. Ed. Engl. 29:992-1023.
79. van Gunsteren, W. F., S. R. Billeter, A. A. Eising, P. H. Hünenberger, P. Krüger, A. E. Mark, W. R. P. Scott, and I. G. Tironi. 1996. Biomolecular Simulation: The GROMOS96 Manual and User Guide. Hochschulverlag an der ETH Zürich/Biomos, Zürich/Groningen.
80. Westh, P., and H. Ramlov. 1991. Trehalose accumulation in the tardigrade adorybiotus-coronifer during anhydrobiosis. J. Exp. Zool. 258:303-311.
81. Williams, R. J., and A. C. Leopold. 1989. The glassy state in com embryos. Plant Physiol. 89:977-981.
82. Wingler, A. 2002. The function of trehalose biosynthesis in plants. Phytochemistry. 60:437-440.
83. Wolfe, J., and G. Bryant. 1999. Freezing, drying and or vitrification of membrane-solute-water systems. Cryobiology. 39:103-129.
84. Wyatt, G. R., and G. F. Kalf. 1957. The chemistry of isect hemolymph. 2. Trehalose and other carbohydrates. J. Gen. Physiol. 40:833-847.
85. Xie, G. F., and S. N. Timasheff. 1997. The thermodynamic mechanism of protein stabilization by trehalose. Biophys. Chem. 64:25-43.
86. Zhang, J., and P. L. Steponkus. 1996. Proposed mechanism for depression of the liquid-crystalline-to-gel phase transition temperature of phospholipids in dehydrated sugar-phospholipid mixtures. Cryobiology. 33: 625-626.