Skip to main content
SpringerLink
Log in

Rigidity and spontaneous curvature of lipidic monolayers in the presence of trehalose: a measurement in the DOPE inverted hexagonal phase

  • Article
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

Trehalose is a sugar which plays an important protectant role in organisms against damage due to dehydration. To explore the basic molecular mechanism which governs the protective function exerted on lipid membranes, X-ray diffraction and osmotic stress experiments have been performed on l-α-dioleoyl-phosphatidyl-ethanolamine (DOPE) in trehalose solutions of different concentrations. In pure water, DOPE forms an inverted hexagonal (HII) phase; in sugar solutions, a strong dehydration, which induces a large reduction of the HII lattice parameter, has been detected, but nevertheless no phase transitions occur. Structural data, directly obtained from reconstructed electron density maps, show that the bending of the lipid monolayer induced by the sugar is coupled to changes in the DOPE molecular shape. By osmotic stress, the work required to dehydrate the monolayer has been obtained and the overall free energy described as a function of trehalose concentration. Three results should be stressed: (1) dehydration experiments performed in the presence of sugar demonstrate that the protective effect cannot be purely osmotic; (2) the pivotal surface, that location on the molecule whose area is invariant upon isothermal bending, has been analyzed by two different methods: the approach by Rand and co-workers and the approach by Templer and co-workers; in both cases its presence along the DOPE molecule has been revealed and its position estimated; (3) the spontaneous radius of curvature and the rigidity constant of the lipid monolayer, measured at the pivotal plane, changes from 3.06 nm (in pure water) to 2.82 nm (in 1.4 M trehalose), and from 0.55×10−19 to 0.74×10−19 J, respectively. We assume that these modifications are related to direct interactions between trehalose and DOPE that alter the interface geometry, reducing the repulsion between the polar heads. However, the increased bending rigidity also accounts for the changes of the property of the aqueous compartment, reflecting the rigidity and stiffness of the sugar matrix around and inside the lipid phase.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16

Similar content being viewed by others

References

  • Branca C, Magazù S, Migliardo F, Migliardo P (2002) Destructuring effect of trehalose on the tetrahedral network of water: a Raman and neutron diffraction comparison. Physica A 304:314–318

    Article  CAS  Google Scholar 

  • Cevc G (1991) Polymorphism of the bilayer membranes in the ordered phase and the molecular origin of the lipid pretransition and rippled lamellae. Biochim Biophys Acta 1062:59–69

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Rand RP (1998) Comparative study of the effects of several n-alkanes on phospholipid hexagonal phases. Biophys J 74:944–952

    CAS  PubMed  Google Scholar 

  • Collins KD, Washabaugh MW (1985) The Hofmeister effect and the behaviour of water at interfaces. Q Rev Biophys 18:323–422

    CAS  PubMed  Google Scholar 

  • Cordone L, Galajda P, Vitrano E, Gassmann A, Ostermann A, Parak F (1998) A reduction of protein specific motions in coligated myoglobin embedded in trehalose glass. Eur Biophys J 27:173–176

    Article  CAS  PubMed  Google Scholar 

  • Cottone G, Ciccotti G, Cordone L (2002) Protein-trehalose-water structures in trehalose coated carboxy-myoglobin. J Chem Phys 117:9862–9866

    Article  CAS  Google Scholar 

  • Crowe JH, Crowe LM (1988) Trehalose and dry dipalmitoyl phosphatidylcholine revisited. Biochim Biophys Acta 946:193–201

    Article  CAS  PubMed  Google Scholar 

  • Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703

    CAS  Google Scholar 

  • Crowe LM (2002) Lessons from nature: the role of sugars in anhydrobiosis. Comp Biochem Physiol A 131:505–513

    Article  Google Scholar 

  • Crowe LM, Crowe JH, Carpenter JF, Wistrom CA (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242:1–10

    CAS  PubMed  Google Scholar 

  • Evans E, Needham D (1987) Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion and colloidal interactions. J Phys Chem 91:4219–4228

    CAS  Google Scholar 

  • Fuller N, Rand RP (2001) The influence of lysolipids on the spontaneous curvature and bending elasticity of phospholipid membranes. Biophys J 81:243–254

    CAS  PubMed  Google Scholar 

  • Gawrish K, Parsegian VA, Hajduk DA, Tate MW, Gruner SM, Fuller NL, Rand RP (1992) Energetics of a hexagonal-kamellar-hexagonal phase transition sequence in dioleoylphosphatidylethanolamine membranes. Biochemistry 31:2856–2864

    PubMed  Google Scholar 

  • Harper PE, Mannock DA, Lewis RNAH, McElhaney RN, Gruner SM (2001) X-ray diffraction structures of some phosphatidylethanolamine lamellar and inverted hexagonal phases. Biophys J 81:2693–2706

    CAS  PubMed  Google Scholar 

  • Heerklotz H, Seelig J (2002) Application of pressure perturbation calorimetry to lipid bilayers. Biophis J 82:1445–1452

    CAS  Google Scholar 

  • Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C 28:693–703

    CAS  PubMed  Google Scholar 

  • Koynova R, Caffrey M (1994) Phases and phase transitions of the hydrated phosphatidylethanolamines. Chem Phys Lipids 62:253–262

    Google Scholar 

  • Koynova RD, Tenchov BG, Quinn PJ (1989) Sugars favor formation of hexagonal phase at the expense of the lamellar liquid-crystalline phase in hydrated phosphatidylethanolamines. Biochim Biophys Acta 980:377–380

    Article  Google Scholar 

  • Koynova R, Brankov J, Tenchov B (1997) Modulation of the lipid phase behaviour by kosmotropic and chaotropic solutes. Eur Biophys J 25:261–275

    Article  CAS  Google Scholar 

  • Kozlov MM, Winterhalter M (1991) Elastic moduli for strongly curved monolayers. Position of the neutral surface. J Phys II (France) 1:1077–1084

    Google Scholar 

  • Kozlov MM, Leikin S, Rand RP (1994) Bending, hydration and interstitial energies quantitatively account for the hexagonal-lamellar-hexagonal reentrant phase transition in dioleoyl phosphatidyl ethanolamine. Biophys J 67:1603–1611

    CAS  PubMed  Google Scholar 

  • Leikin S, Kozlov MM, Fuller NL, Rand RP (1996) Measured effects of diacylglycerol on structural and elastic properties of phospholipid membranes. Biophys J 71:2623–2632

    CAS  PubMed  Google Scholar 

  • Librizzi FC, Viappiani C, Abbruzzetti S, Cordone L (2002) Residual water modulates the dynamics of the protein and of the external matrix in “trehalose coated” MbCO: an infrared and flash photolysis study. J Chem Phys 116:1193–1200

    Article  CAS  Google Scholar 

  • Lide DR (1996) Handbook of chemistry and physics, 77th edn. CRC, Boca Raton

  • Luzzati V (1968) X-ray diffraction studies of lipid-water systems. In: Chapman D (ed) Biological Membranes, vol 1, chap 3. Academic Press, London, pp 71–123

  • Mariani P, Luzzati V, Delacroix H (1988) Cubic phases of lipid-containing systems. Structure analysis and biological implications. J Mol Biol 204:165–189

    CAS  PubMed  Google Scholar 

  • Mariani P, Rustichelli F, Saturni L, Cordone L (1999) Stabilization of the monoolein Pn3m cubic structure on trehalose glasses. Eur Biophys J 28:294–301

    Article  CAS  Google Scholar 

  • Parsegian VA, Rand RP, Fuller NL, Rau DC (1986) Osmotic stress for the direct measurement of intermolecular forces. Methods Enzymol 127:400–416

    Article  CAS  PubMed  Google Scholar 

  • Perry RN, Clarke AJ, Hennessy J (1980) The influence of osmotic pressure on the hatching of Heterodera schachtii. Rev Nematol 3(1):3–9

    Google Scholar 

  • Rand RP, Fuller NL (1994) Structural dimensions and their changes in a reentrant hexagonal-lamellar transition of phospholipids. Biophys J 66:2127–2138

    CAS  PubMed  Google Scholar 

  • Rand RP, Fuller NL, Parsegian VA, Rau DC (1988) Variation in hydration forces between neutral phospholipid bilayer: evidence for hydration attraction. Biochemistry 27:7711–22

    CAS  PubMed  Google Scholar 

  • Rand RP, Fuller NL, Gruner SM, Parsegian VA (1990) Membrane curvature, lipid segregation and structural transitions for phospholipids under dual-solvent stress. Biochemistry 29:76–87

    CAS  PubMed  Google Scholar 

  • Rappolt M, Hickel A, Bringezu F, Lohner K (2003) Mechanism of the lamellar/inverse hexagonal phase transition examined by high resolution X-ray diffraction. Biophys J 84:3111–3122

    CAS  PubMed  Google Scholar 

  • Rau DC, Parsegian VA (1992) Direct measurement of the intermolecular forces between counterion-condensed DNA double helices. Evidence for long range attractive hydration forces. Biophys J 61:246–259

    CAS  PubMed  Google Scholar 

  • Rau DC, Lee B, Parsegian VA (1984) Measurement of the repulsive force between polyelectrolyte molecules in ionic solution: hydration forces between parallel DNA double helices. Proc Natl Acad Sci USA 81:2821–2825

    PubMed  Google Scholar 

  • Rector D, Jiang J, Berg MA, Fayer MD (2001) Effects of solvent viscosity on protein dynamics: infrared vibrational echo experiments and theory. J Phys Chem B 105:1081–1092

    Article  CAS  Google Scholar 

  • Salmon A, Dodd W, Williams GD, Beach JM, Brown MF (1987) Configurational statistics of acyl chains in polyunsaturated lipid bilayers from H-2 NMR. J Am Chem Soc 109:2600–2609

    CAS  Google Scholar 

  • Sanderson PW, Lis LJ, Quinn PJ, Williams WP (1991) The Hofmeister effect in relation to membrane lipid phase stability. Biochim Biophys Acta 1067:43–50

    Article  CAS  PubMed  Google Scholar 

  • Sankaram MB, Thompson TE (1992) Deuterium magnetic resonance study of phase equilibria and membrane thickness in binary phospholipid mixed bilayers. Biochemistry 31:8258–8268

    CAS  PubMed  Google Scholar 

  • Saturni L, Rustichelli F, Di Gregorio GM, Cordone L, Mariani P (2001) Sugar-induced stabilization of the monoolein Pn3m bicontinuous cubic phase during dehydration. Phys Rev E 64:0409021–4

    Article  Google Scholar 

  • Seelig J, Seelig A (1974) Deuterium magnetic resonance studies of phospholipid bilayers. Biochem Biophys Res Commun 57:406–411

    CAS  PubMed  Google Scholar 

  • Shalaev EY, Steponkus PL (2001) Phase behavior and glass transition of 1,2-dioleoylphosphatidylethanolamine (DOPE) dehydrated in the presence of sucrose. Biochim Biophys Acta 1514:100–116

    Article  CAS  PubMed  Google Scholar 

  • Szule JA, Rand RP (2003) The effects of gramicidin on the structure of phospholipid assemblies. Biophys J 85:1702–1712

    CAS  PubMed  Google Scholar 

  • Takahashi H, Ohmae H, Hatta I (1997) Trehalose-induced destabilization of interdigitated gel phase in dihexadecylphosphatidylcholine. Biophys J 73:3030–3038

    CAS  PubMed  Google Scholar 

  • Templer RH, Turner DC, Harper P, Seddon JM (1995) Corrections to some models of the curvature elastic energy of inverse bicontinuous cubic phases. J Phys II (France) 5:1053–1065

    Google Scholar 

  • Templer RH, Seddon JM, Warrender NA, Syrykh A, Huang Z, Winter R, Erbes J (1998) Inverse bicontinuous cubic phases in 2:1 fatty acid/phosphatidylcholine mixtures. The effects of chain length, hydration, and temperature. J Phys Chem 102:7251–7261

    Article  CAS  Google Scholar 

  • Tenchov B, Koynova R, Rapp G (2001) New ordered metastable phases between the gel and subgel phases in hydrated phospholipids. Biophys J 80:1873–1890

    CAS  PubMed  Google Scholar 

  • Tsonev LI, Tihova MG, Brain APR, Yu Z-W, Quinn PJ (1994) The effect of cryoprotective sugar, trehalose, on the phase behaviour of mixed dispersions of dioleoyl derivatives of phosphatidylethanolamine and phosphatidylcholine. Liq Cryst 17:717–728

    CAS  Google Scholar 

  • Turner DC, Gruner SM (1992) X-ray diffraction reconstruction of the inverted hexagonal (HII) phase in lipid-water systems. Biochemistry 31:1340–1355

    CAS  PubMed  Google Scholar 

  • Vacklin H, Khoo BJ, Madan KH, Seddon JM, Templer RH (2000) The bending elasticity of 1-monoolein upon relief of packing stress. Langmuir 16:4741–4748

    Article  CAS  Google Scholar 

  • Wistrom CA, Rand RP, Growe LM, Spargo BJ, Crowe JH (1989) Direct transition of dioleoylphosphatidylethanolamine from lamellar gel to inverted hexagonal phase caused by trehalose. Biochim Biophys Acta 984:238–242

    CAS  Google Scholar 

  • Zhang J, Steponkus PL (1996) Proposed mechanism for depression of the liquid-crystalline-to-gel phase transition temperature of phospholipids in dehydrated sugar-phospholipids mixtures. Cryobiology 33:21A

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dipartimento di Scienze Applicate ai Sistemi Complessi, Università Politecnica delle Marche and INFM, via Ranieri 65, 60131 , Ancona, Italy

    Giordano M. Di Gregorio & Paolo Mariani

Authors
  1. Giordano M. Di Gregorio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paolo Mariani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paolo Mariani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Di Gregorio, G.M., Mariani, P. Rigidity and spontaneous curvature of lipidic monolayers in the presence of trehalose: a measurement in the DOPE inverted hexagonal phase. Eur Biophys J 34, 67–81 (2005). https://doi.org/10.1007/s00249-004-0425-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-004-0425-0

Keywords

Search

Navigation