Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1987 Feb 15;242(1):1–10. doi: 10.1042/bj2420001

Stabilization of dry phospholipid bilayers and proteins by sugars.

J H Crowe, L M Crowe, J F Carpenter, C Aurell Wistrom
PMCID: PMC1147656  PMID: 2954537

Full text

PDF
1

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahkong Q. F., Fisher D., Tampion W., Lucy J. A. Mechanisms of cell fusion. Nature. 1975 Jan 17;253(5488):194–195. doi: 10.1038/253194a0. [DOI] [PubMed] [Google Scholar]
  2. Arakawa T., Timasheff S. N. Stabilization of protein structure by sugars. Biochemistry. 1982 Dec 7;21(25):6536–6544. doi: 10.1021/bi00268a033. [DOI] [PubMed] [Google Scholar]
  3. Back J. F., Oakenfull D., Smith M. B. Increased thermal stability of proteins in the presence of sugars and polyols. Biochemistry. 1979 Nov 13;18(23):5191–5196. doi: 10.1021/bi00590a025. [DOI] [PubMed] [Google Scholar]
  4. Baudier J., Haglid K., Haiech J., Gérard D. Zinc ion binding to human brain calcium binding proteins, calmodulin and S100b protein. Biochem Biophys Res Commun. 1983 Aug 12;114(3):1138–1146. doi: 10.1016/0006-291x(83)90681-2. [DOI] [PubMed] [Google Scholar]
  5. Blok M. C., van der Neut-Kok E. C., van Deenen L. L., de Gier J. The effect of chain length and lipid phase transitions on the selective permeability properties of liposomes. Biochim Biophys Acta. 1975 Oct 6;406(2):187–196. doi: 10.1016/0005-2736(75)90003-6. [DOI] [PubMed] [Google Scholar]
  6. Boni L. T., Stewart T. P., Hui S. W. Alterations in phospholipid polymorphism by polyethylene glycol. J Membr Biol. 1984;80(1):91–104. doi: 10.1007/BF01868693. [DOI] [PubMed] [Google Scholar]
  7. Bramhall J. Phospholipid packing asymmetry in curved membranes detected by fluorescence spectroscopy. Biochemistry. 1986 Jun 3;25(11):3479–3486. doi: 10.1021/bi00359a057. [DOI] [PubMed] [Google Scholar]
  8. Büldt G., Gally H. U., Seelig A., Seelig J., Zaccai G. Neutron diffraction studies on selectively deuterated phospholipid bilayers. Nature. 1978 Jan 12;271(5641):182–184. doi: 10.1038/271182a0. [DOI] [PubMed] [Google Scholar]
  9. CHILSON O. P., COSTELLO L. A., KAPLAN N. O. EFFECTS OF FREEZING ON ENZYMES. Fed Proc. 1965 Mar-Apr;24:S55–S65. [PubMed] [Google Scholar]
  10. Carpenter J. F., Hand S. C., Crowe L. M., Crowe J. H. Cryoprotection of phosphofructokinase with organic solutes: characterization of enhanced protection in the presence of divalent cations. Arch Biochem Biophys. 1986 Nov 1;250(2):505–512. doi: 10.1016/0003-9861(86)90755-1. [DOI] [PubMed] [Google Scholar]
  11. Crowe J. H., Crowe L. M., Chapman D. Infrared spectroscopic studies on interactions of water and carbohydrates with a biological membrane. Arch Biochem Biophys. 1984 Jul;232(1):400–407. doi: 10.1016/0003-9861(84)90555-1. [DOI] [PubMed] [Google Scholar]
  12. Crowe J. H., Crowe L. M., Chapman D. Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science. 1984 Feb 17;223(4637):701–703. doi: 10.1126/science.223.4637.701. [DOI] [PubMed] [Google Scholar]
  13. Crowe J. H., Crowe L. M., Jackson S. A. Preservation of structural and functional activity in lyophilized sarcoplasmic reticulum. Arch Biochem Biophys. 1983 Feb 1;220(2):477–484. doi: 10.1016/0003-9861(83)90438-1. [DOI] [PubMed] [Google Scholar]
  14. Crowe L. M., Crowe J. H., Chapman D. Interaction of carbohydrates with dry dipalmitoylphosphatidylcholine. Arch Biochem Biophys. 1985 Jan;236(1):289–296. doi: 10.1016/0003-9861(85)90628-9. [DOI] [PubMed] [Google Scholar]
  15. Crowe L. M., Crowe J. H. Hydration-dependent hexagonal phase lipid in a biological membrane. Arch Biochem Biophys. 1982 Sep;217(2):582–587. doi: 10.1016/0003-9861(82)90540-9. [DOI] [PubMed] [Google Scholar]
  16. Crowe L. M., Crowe J. H., Rudolph A., Womersley C., Appel L. Preservation of freeze-dried liposomes by trehalose. Arch Biochem Biophys. 1985 Oct;242(1):240–247. doi: 10.1016/0003-9861(85)90498-9. [DOI] [PubMed] [Google Scholar]
  17. Crowe L. M., Mouradian R., Crowe J. H., Jackson S. A., Womersley C. Effects of carbohydrates on membrane stability at low water activities. Biochim Biophys Acta. 1984 Jan 11;769(1):141–150. doi: 10.1016/0005-2736(84)90017-8. [DOI] [PubMed] [Google Scholar]
  18. Darbyshire B. The function of the carbohydrate units of three fungal enzymes in their resistance to dehydration. Plant Physiol. 1974 Nov;54(5):717–721. doi: 10.1104/pp.54.5.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ebihara L., Hall J. E., MacDonald R. C., McIntosh T. J., Simon S. A. Effect of benzyl alcohol on lipid bilayers. A comparisons of bilayer systems. Biophys J. 1979 Nov;28(2):185–196. doi: 10.1016/S0006-3495(79)85170-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gaskin F., Kress Y. Zinc ion-induced assembly of tubulin. J Biol Chem. 1977 Oct 10;252(19):6918–6924. [PubMed] [Google Scholar]
  21. Gruner S. M. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3665–3669. doi: 10.1073/pnas.82.11.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hammoudah M. M., Nir S., Bentz J., Mayhew E., Stewart T. P., Hui S. W., Kurland R. J. Interactions of La2+ with phosphatidylserine vesicles: binding, phase transition, leakage, 31P-NMR and fusion. Biochim Biophys Acta. 1981 Jul 6;645(1):102–114. doi: 10.1016/0005-2736(81)90517-4. [DOI] [PubMed] [Google Scholar]
  23. Hauser H., Pascher I., Pearson R. H., Sundell S. Preferred conformation and molecular packing of phosphatidylethanolamine and phosphatidylcholine. Biochim Biophys Acta. 1981 Jun 16;650(1):21–51. doi: 10.1016/0304-4157(81)90007-1. [DOI] [PubMed] [Google Scholar]
  24. Hellman K., Miller D. S., Cammack K. A. The effect of freeze-drying on the quaternary structure of L-asparaginase from Erwinia carotovora. Biochim Biophys Acta. 1983 Dec 12;749(2):133–142. doi: 10.1016/0167-4838(83)90245-5. [DOI] [PubMed] [Google Scholar]
  25. Janiak M. J., Small D. M., Shipley G. G. Temperature and compositional dependence of the structure of hydrated dimyristoyl lecithin. J Biol Chem. 1979 Jul 10;254(13):6068–6078. [PubMed] [Google Scholar]
  26. Khanna N. C., Tokuda M., Waisman D. M. Conformational changes induced by binding of divalent cations to calregulin. J Biol Chem. 1986 Jul 5;261(19):8883–8887. [PubMed] [Google Scholar]
  27. Labrude P., Loppinet V., Vigneron C. [Protective molecules for hemoglobin during lyophilization]. Ann Pharm Fr. 1976 Mar-Apr;34(3-4):143–149. [PubMed] [Google Scholar]
  28. Larsson H., Wallin M., Edström A. Induction of a sheet polymer of tubulin by Zn2+. Exp Cell Res. 1976 Jun;100(1):104–110. doi: 10.1016/0014-4827(76)90332-3. [DOI] [PubMed] [Google Scholar]
  29. Lee A. G. Lipid phase transitions and phase diagrams. I. Lipid phase transitions. Biochim Biophys Acta. 1977 Aug 9;472(2):237–281. doi: 10.1016/0304-4157(77)90018-1. [DOI] [PubMed] [Google Scholar]
  30. Lee A. G. Lipid phase transitions and phase diagrams. II. Mictures involving lipids. Biochim Biophys Acta. 1977 Nov 14;472(3-4):285–344. doi: 10.1016/0304-4157(77)90001-6. [DOI] [PubMed] [Google Scholar]
  31. Lee C. W., Waugh J. S., Griffin R. G. Solid-state NMR study of trehalose/1,2-dipalmitoyl-sn-phosphatidylcholine interactions. Biochemistry. 1986 Jul 1;25(13):3737–3742. doi: 10.1021/bi00361a001. [DOI] [PubMed] [Google Scholar]
  32. Lee J. C., Timasheff S. N. The stabilization of proteins by sucrose. J Biol Chem. 1981 Jul 25;256(14):7193–7201. [PubMed] [Google Scholar]
  33. Lis L. J., McAlister M., Fuller N., Rand R. P., Parsegian V. A. Interactions between neutral phospholipid bilayer membranes. Biophys J. 1982 Mar;37(3):657–665. [PMC free article] [PubMed] [Google Scholar]
  34. MacDonald R. I., MacDonald R. C. Lipid mixing during freeze-thawing of liposomal membranes as monitored by fluorescence energy transfer. Biochim Biophys Acta. 1983 Nov 9;735(2):243–251. doi: 10.1016/0005-2736(83)90299-7. [DOI] [PubMed] [Google Scholar]
  35. Madden T. D., Bally M. B., Hope M. J., Cullis P. R., Schieren H. P., Janoff A. S. Protection of large unilamellar vesicles by trehalose during dehydration: retention of vesicle contents. Biochim Biophys Acta. 1985 Jul 11;817(1):67–74. doi: 10.1016/0005-2736(85)90069-0. [DOI] [PubMed] [Google Scholar]
  36. Mantsch H. H., Martin A., Cameron D. G. Characterization by infrared spectroscopy of the bilayer to nonbilayer phase transition of phosphatidylethanolamines. Biochemistry. 1981 May 26;20(11):3138–3145. doi: 10.1021/bi00514a024. [DOI] [PubMed] [Google Scholar]
  37. Marlborough D. I., Miller D. S., Cammack K. A. Comparative study on conformational stability and subunit interactions of two bacterial asparaginases. Biochim Biophys Acta. 1975 Apr 29;386(2):576–589. doi: 10.1016/0005-2795(75)90301-3. [DOI] [PubMed] [Google Scholar]
  38. Matubayasi N., Shigematsu T., Iehara T., Kamaya H., Ueda I. Miscibility of phosphatidylcholine binary mixtures in unilamellar vesicles: phase equilibria. J Membr Biol. 1986;90(1):37–42. doi: 10.1007/BF01869684. [DOI] [PubMed] [Google Scholar]
  39. Mouradian R., Womersley C., Crowe L. M., Crowe J. H. Degradation of functional integrity during long-term storage of a freeze-dried biological membrane. Cryobiology. 1985 Apr;22(2):119–127. doi: 10.1016/0011-2240(85)90166-x. [DOI] [PubMed] [Google Scholar]
  40. Nickolson V. J., Veldstra H. The influence of various cations on the binding of colchicine by rat brain homogenates. Stabilization of intact neurotubules by zinc and cadmium ions. FEBS Lett. 1972 Jul 1;23(3):309–313. doi: 10.1016/0014-5793(72)80303-x. [DOI] [PubMed] [Google Scholar]
  41. Papahadjopoulos D., Jacobson K., Nir S., Isac T. Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol. Biochim Biophys Acta. 1973 Jul 6;311(3):330–348. doi: 10.1016/0005-2736(73)90314-3. [DOI] [PubMed] [Google Scholar]
  42. Parsegian V. A., Fuller N., Rand R. P. Measured work of deformation and repulsion of lecithin bilayers. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2750–2754. doi: 10.1073/pnas.76.6.2750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Pick U. Liposomes with a large trapping capacity prepared by freezing and thawing of sonicated phospholipid mixtures. Arch Biochem Biophys. 1981 Nov;212(1):186–194. doi: 10.1016/0003-9861(81)90358-1. [DOI] [PubMed] [Google Scholar]
  44. Quinn P. J. A lipid-phase separation model of low-temperature damage to biological membranes. Cryobiology. 1985 Apr;22(2):128–146. doi: 10.1016/0011-2240(85)90167-1. [DOI] [PubMed] [Google Scholar]
  45. Rudolph A. S., Crowe J. H., Crowe L. M. Effects of three stabilizing agents--proline, betaine, and trehalose--on membrane phospholipids. Arch Biochem Biophys. 1986 Feb 15;245(1):134–143. doi: 10.1016/0003-9861(86)90197-9. [DOI] [PubMed] [Google Scholar]
  46. Rudolph A. S., Crowe J. H. Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline. Cryobiology. 1985 Aug;22(4):367–377. doi: 10.1016/0011-2240(85)90184-1. [DOI] [PubMed] [Google Scholar]
  47. Schuh J. R., Banerjee U., Müller L., Chan S. I. The phospholipid packing arrangement in small bilayer vesicles as revealed by proton magnetic resonance studies at 500 MHz. Biochim Biophys Acta. 1982 May 7;687(2):219–225. doi: 10.1016/0005-2736(82)90549-1. [DOI] [PubMed] [Google Scholar]
  48. Simon S. A., McIntosh T. J., Latorre R. Influence of cholesterol on water penetration into bilayers. Science. 1982 Apr 2;216(4541):65–67. doi: 10.1126/science.7063872. [DOI] [PubMed] [Google Scholar]
  49. Simpson R. T., Vallee B. L. Zinc and cobalt alkaline phosphatases. Ann N Y Acad Sci. 1969 Oct 14;166(2):670–695. doi: 10.1111/j.1749-6632.1969.tb46426.x. [DOI] [PubMed] [Google Scholar]
  50. Strauss G., Hauser H. Stabilization of lipid bilayer vesicles by sucrose during freezing. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2422–2426. doi: 10.1073/pnas.83.8.2422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Strauss G., Schurtenberger P., Hauser H. The interaction of saccharides with lipid bilayer vesicles: stabilization during freeze-thawing and freeze-drying. Biochim Biophys Acta. 1986 Jun 13;858(1):169–180. doi: 10.1016/0005-2736(86)90303-2. [DOI] [PubMed] [Google Scholar]
  52. Suurkuusk J., Lentz B. R., Barenholz Y., Biltonen R. L., Thompson T. E. A calorimetric and fluorescent probe study of the gel-liquid crystalline phase transition in small, single-lamellar dipalmitoylphosphatidylcholine vesicles. Biochemistry. 1976 Apr 6;15(7):1393–1401. doi: 10.1021/bi00652a007. [DOI] [PubMed] [Google Scholar]
  53. Thirion C., Larcher D., Chaillot B., Labrude P., Vigneron C. Circular dichroism studies of freeze-drying-induced conformational changes in human hemoglobin. Biopolymers. 1983 Nov;22(11):2367–2381. doi: 10.1002/bip.360221105. [DOI] [PubMed] [Google Scholar]
  54. Uster P. S., Deamer D. W. Fusion competence of phosphatidylserine-containing liposomes quantitatively measured by a fluorescence resonance energy transfer assay. Arch Biochem Biophys. 1981 Jul;209(2):385–395. doi: 10.1016/0003-9861(81)90296-4. [DOI] [PubMed] [Google Scholar]
  55. White S. H. Studies of the physical chemistry of planar bilayer membranes using high-precision measurements of specific capacitance. Ann N Y Acad Sci. 1977 Dec 30;303:243–265. [PubMed] [Google Scholar]
  56. Whittam J. H., Rosano H. L. Effects of the freeze-thaw process on alpha amylase. Cryobiology. 1973 Aug;10(3):240–243. doi: 10.1016/0011-2240(73)90037-0. [DOI] [PubMed] [Google Scholar]
  57. Womersley C., Uster P. S., Rudolph A. S., Crowe J. H. Inhibition of dehydration-induced fusion between liposomal membranes by carbohydrates as measured by fluorescence energy transfer. Cryobiology. 1986 Jun;23(3):245–255. doi: 10.1016/0011-2240(86)90050-7. [DOI] [PubMed] [Google Scholar]
  58. Zaccai G., Büldt G., Seelig A., Seelig J. Neutron diffraction studies on phosphatidylcholine model membranes. II. Chain conformation and segmental disorder. J Mol Biol. 1979 Nov 15;134(4):693–706. doi: 10.1016/0022-2836(79)90480-7. [DOI] [PubMed] [Google Scholar]
  59. van Dijck P. W., de Kruijff B., Aarts P. A., Verkleij A. J., de Gier J. Phase transitions in phospholipid model membranes of different curvature. Biochim Biophys Acta. 1978 Jan 19;506(2):183–191. doi: 10.1016/0005-2736(78)90389-9. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES