Skip to main content
SpringerLink
Log in

The effects of cholesterol and β-sitosterol on the structure of saturated diacylphosphatidylcholine bilayers

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

The structures of DMPC and DPPC bilayers in unilamellar liposomes, in the presence of 33.3 mol% cholesterol or the plant sterol β-sitosterol, have been studied by small-angle neutron scattering. The bilayer thickness d L increases in a similar way for both sterols. The repeat distance in multilamellar liposomes, as determined by small-angle X-ray diffraction, is larger in the presence of β-sitosterol than in the presence of cholesterol. We observe that each sterol modifies the interlamellar water layer differently, cholesterol reducing its thickness more efficiently than β-sitosterol, and conclude that cholesterol suppresses bilayer undulations more effectively than β-sitosterol.

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

Similar content being viewed by others

Abbreviations

DLPC:

1,2-dilauroyl-sn-glycero-3-phosphatidylcholine

DMPC:

1,2-dimyristoyl-sn-glycero-3-phosphatidylcholine

DPPC:

1,2-dipalmitoyl-sn-glycero-3-phosphatidylcholine

DSPC:

1,2-distearoyl-sn-glycero-3-phosphatidylcholine

SANS:

Small-angle neutron scattering

SAXD:

Small-angle X-ray diffraction

Chol:

Cholesterol

Sit:

β-sitosterol

TMA-DPH:

1-(4-trimethylammonium-phenyl)-6-phenyl-1,3,5-hexatriene

References

  • Almeida PFF, Vaz WLC, Thompson TE (1992) Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine cholesterol lipid bilayers––a free-volume analysis. Biochemistry 31:6739–6747

    Article  CAS  PubMed  Google Scholar 

  • Awad AB, Fink CS (2000) Phytosterols as anticancer dietary components: evidence and mechanism of action. J Nutr 130:2127–2130

    CAS  PubMed  Google Scholar 

  • Balgavý P, Dubničková M, Kučerka N, Kiselev MA, Yaradaikin SP, Uhríková D (2001) Bilayer thickness and lipid interface area in unilamellar extruded 1,2-diacylphosphatidylcholine liposomes: a small-angle neutron scattering study. Biochim Biophys Acta 1512:40–52

    Article  PubMed  Google Scholar 

  • Beck JG, Mathieu D, Loudet C, Buchoux S, Dufourc EJ (2007) Plant sterols in “rafts”: a better way to regulate membrane thermal shocks. FASEB J 21:1714–1723

    Article  CAS  PubMed  Google Scholar 

  • Bernsdorff C, Winter R (2003) Differential properties of the sterols cholesterol, ergosterol, beta-sitosterol, trans-7-dehydrocholesterol, stigmasterol and lanosterol on DPPC bilayer order. J Phys Chem B 107:10658–10664

    Article  CAS  Google Scholar 

  • Bigi A, Roveri N (1991) Fibre diffraction: collagen. In: Ebashi S, Koch M, Rubenstein E (eds) Handbook on Synchrotron Radiation. Elsevier Science Publisher B.V., Amsterdam

    Google Scholar 

  • Bradford PG, Awad AB (2007) Phytosterols as anticancer compounds. Mol Nutr Food Res 51:161–170

    Article  CAS  PubMed  Google Scholar 

  • Cevc G (1993) Phospholipids Handbook. Marcel Dekker, Inc., New York

    Google Scholar 

  • Clarke JA, Heron AJ, Seddon JM, Law RV (2006) The diversity of the liquid ordered (Lo) phase of phosphatidylcholine/cholesterol membranes: a variable temperature multinuclear solid-state NMR and X-ray diffraction study. Biophys J 90:2383–2393

    Article  CAS  PubMed  Google Scholar 

  • Faure C, Tranchant JF, Dufourc EJ (1996) Comparative effects of cholesterol and cholesterol sulfate on hydration and ordering of dimyristoylphosphatidylcholine membranes. Biophys J 70:1380–1390

    Article  CAS  PubMed  Google Scholar 

  • Gallová J, Uhríková D, Kučerka N, Teixeira J, Balgavý P (2008) Hydrophobic thickness, lipid surface area and polar region hydration in monounsaturated diacylphosphatidylcholine bilayers: SANS study of effects of cholesterol and β-sitosterol. Biochim Biophys Acta 1778:2627–2632

    Article  PubMed  Google Scholar 

  • Gao W, Chen L, Wu F, Yu Z (2008) Liquid ordered phase of binary mixtures containing dipalmitoylphosphatidylcholine and sterols. Acta Phys-Chim Sin 24:1149–1154

    Article  CAS  Google Scholar 

  • Gordeliy V, Golubchikova LV, Kuklin A, Syrykh AG, Watts A (1993) The study of single biological and model membranes via small-angle neutron scattering. Progr Colloid Polym Sci 93:252–257

    Article  CAS  Google Scholar 

  • Hac-Wydro K, Wydro P, Jagoda A, Kapusta J (2007) The study on the interaction between phytosterols and phospholipids in model membranes. Chem Phys Lipids 150:22–34

    Article  CAS  PubMed  Google Scholar 

  • Hodzic A, Rappolt M, Amenitsch H, Laggner P, Pabst G (2008) Differential modulation of membrane structure and fluctuations by plant sterols and cholesterol. Biophys J 94:3935–3944

    Article  CAS  PubMed  Google Scholar 

  • Huang JY, Feigenson GW (1999) A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys J 76:2142–2157

    Article  CAS  PubMed  Google Scholar 

  • Hung WC, Lee MT, Chen FY, Huang HW (2007) The condensing effect of cholesterol in lipid bilayers. Biophys J 92:3960–3967

    Article  CAS  PubMed  Google Scholar 

  • Ipsen JH, Karlström G, Mouritsen OG, Wennerström H, Zuckermann MJ (1987) Phase equilibria in the phosphatidylcholine–cholesterol system. Biochim Biophys Acta 905:162–172

    Article  CAS  PubMed  Google Scholar 

  • Janiak MJ, Small DM, Shipley GG (1976) Nature of the thermal pretransition of synthetic phospholipids: dimyristoyl- and dipalmitoyllecithin. Biochemistry 15:4575–4580

    Article  CAS  PubMed  Google Scholar 

  • Korstanje LJ, Vanginkel G, Levine YK (1990) Effects of steroid molecules on the dynamic structure of dioleoylphosphatidylcholine and digalactosyldiacylglycerol bilayers. Biochim Biophys Acta 1022:155–162

    Article  CAS  PubMed  Google Scholar 

  • Kučerka N, Uhríková D, Teixeira J, Balgavý P (2003) Lipid bilayer thickness in extruded liposomes prepared from 1,2-diacylphosphatidylcholines with monounsaturated acyl chains: a small-angle neutron scattering study. Acta Facult Pharm Univ Comenianae 50:78–89

    Google Scholar 

  • Kučerka N, Nagle JF, Feller SE, Balgavý P (2004a) Models to analyze small-angle neutron scattering from unilamellar lipid vesicles. Phys Rev E 69:051903

    Article  Google Scholar 

  • Kučerka N, Kiselev MA, Balgavý P (2004b) Determination of bilayer thickness and lipid surface area in unilamellar dimyristoylphosphatidylcholine vesicles from small-angle neutron scattering curves: a comparison of evaluation methods. Eur Biophys J 33:328–334

    Article  PubMed  Google Scholar 

  • Kučerka N, Pencer J, Nieh MP, Katsaras J (2007) Influence of cholesterol on the bilayer properties of monounsaturated phosphatidylcholine unilamellar vesicles. Eur Phys J 23:247–254

    Google Scholar 

  • Kusumi A, Subczynski WK, Pasenkiewicz-Gierula M, Hyde JS, Merkle H (1986) Spin-label studies on phosphatidylcholine–cholesterol membranes––effects of alkyl chain length and unsaturation in the fluid phase. Biochim Biophys Acta 854:307–317

    Article  CAS  PubMed  Google Scholar 

  • Leonard A, Escrive C, Laguerre M, Pebay-Peyroula E, Neri W, Pott T, Katsaras J, Dufourc EJ (2001) Location of cholesterol in DMPC membranes. A comparative study by neutron diffraction and molecular mechanics simulation. Langmuir 17:2019–2030

    Article  CAS  Google Scholar 

  • MacDonald RC, MacDonald RI, Menco BPM, Takeshita K, Subbarao NK, Hu LR (1991) Small-volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim Biophys Acta 1061:297–303

    Article  CAS  PubMed  Google Scholar 

  • Marsh D, Smith ICP (1973) An interacting spin label study of the fluidizing and condensing effect of cholesterol on lecithin bilayers. Biochim Biophys Acta 298:133–144

    Article  CAS  PubMed  Google Scholar 

  • McIntosh TJ (1978) The effect of cholesterol on the structure of phosphatidylcholine bilayers. Biochim Biophys Acta 513:43–58

    Article  CAS  PubMed  Google Scholar 

  • McKersie BD, Thompson JE (1979) Influence of plant sterols on the phase properties of phospholipid bilayers. Plant Physiol 63:802–805

    Article  CAS  PubMed  Google Scholar 

  • Miao L, Nielsen M, Thewalt J, Ipsen JH, Bloom M, Zuckermann MJ, Mouritsen OG (2002) From lanosterol to cholesterol: structural evolution and differential effects on lipid bilayers. Biophys J 82:1429–1444

    Article  CAS  PubMed  Google Scholar 

  • Mills TT, Huang J, Feigenson GW, Nagle JF (2009) Effect of cholesterol and unsaturated DOPC lipid on chain packing of saturated gel-phase DPPC bilayers. Gen Physiol Biophys 28:126–139

    Article  CAS  PubMed  Google Scholar 

  • Mouritsen OG, Zuckermann MJ (2004) What’s so special about cholesterol? Lipids 39:1101–1113

    Article  CAS  PubMed  Google Scholar 

  • Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta 1469:159–195

    CAS  PubMed  Google Scholar 

  • Nawroth T, Conrad H, Dose K (1989) Neutron small-angle scattering of liposomes in the presence of detergents. Physica B 156:477–480

    Article  Google Scholar 

  • Oradd G, Shahedi V, Lindblom G (2009) Effect of sterol structure on the bending rigidity of lipid membranes: a H-2 NMR transverse relaxation study. Biochim Biophys Acta 1788:1762–1771

    Article  PubMed  Google Scholar 

  • Ovesná Z, Vachálková A, Horváthová K (2004) Taraxasterol and beta-sitosterol: new naturally compounds with chemoprotective/chemopreventive effects. Neoplasma 51:407–414

    PubMed  Google Scholar 

  • Pan JJ, Mills TT, Tristram-Nagle S, Nagle JF (2008) Cholesterol perturbs lipid bilayers nonuniversally. Phys Rev Lett 100:198103

    Article  PubMed  Google Scholar 

  • Pan J, Tristram-Nagle S, Nagle JF (2009) Effect of cholesterol on structural and mechanical properties of membranes depends on lipid chain saturation. Phys Rev E 80:021931

    Article  Google Scholar 

  • Pencer J, Nieh MP, Harroun TA, Krueger S, Adams C, Katsaras J (2005) Bilayer thickness and thermal response of dimyristoylphosphatidylcholine unilamellar vesicles containing cholesterol, ergosterol and lanosterol: a small-angle neutron scattering study. Biochim Biophys Acta 1720:84–91

    Article  CAS  PubMed  Google Scholar 

  • Petrache HI, Harries D, Parsegian VA (2004) Alteration of lipid membrane rigidity by cholesterol and its metabolic precursors. Macromolec Symposia 219:39–50

    Article  CAS  Google Scholar 

  • Rappolt M, Rapp G (1996) Structure of the stable and metastable ripple phase of dipalmitoylphosphatidylcholine. Eur Biophys J 24:381–386

    Article  CAS  Google Scholar 

  • Richter F, Finegold L, Rapp G (1999) Sterols sense swelling in lipid bilayers. Phys Rev E 59:3483–3491

    Article  CAS  Google Scholar 

  • Schreier-Muccillo S, Marsh D, Dugas H, Schneider H, Smith ICP (1973) A spin probe study of the influence of cholesterol on motion and orientation of phospholipid in oriented multilayers and vesicles. Chem Phys Lipids 10:11–27

    Article  CAS  PubMed  Google Scholar 

  • Su Y, Li QZ, Chen L, Yu ZW (2007) Condensation effect of cholesterol, stigmasterol and sitosterol on dipalmitoylphosphatidylcholine in molecular monolayers. Colloids Surf A Physicochem Eng Asp 293:123–129

    Article  CAS  Google Scholar 

  • Tenchov BG, Yao H, Hatta I (1989) Time-resolved X-ray-diffraction and calorimetric studies at low scan rates.1. Fully hydrated dipalmitoylphosphatidylcholine (Dppc) and Dppc/water ethanol phases. Biophys J 56:757–768

    Article  CAS  PubMed  Google Scholar 

  • Uhríková D, Rapp G, Balgavý P (2002) Condensed lamellar phase in ternary DNA-DLPC-cationic gemini surfactant system: a small-angle synchrotron X-ray diffraction study. Bioelectrochemistry 58:87–95

    Article  PubMed  Google Scholar 

  • Urbina JA, Pekerar S, Le HB, Patterson J, Montez B, Oldfield E (1995) Molecular order and dynamics of phosphatidylcholine bilayer membranes in the presence of cholesterol, ergosterol and lanosterol: a comparative study using 2H-, 13C- and 31P-NMR spectroscopy. Biochim Biophys Acta 1238:163–176

    Article  PubMed  Google Scholar 

  • Vist MR, Davis JH (1990) Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry 29:451–464

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the European Commission through the Access Activities of the Integrated Infrastructure Initiative for Neutron Scattering and Muon Spectroscopy (NMI3), supported by the European Commission under the 6th Framework Programme through the Key Action: Strengthening the European Research Area, Research Infrastructures, contract no.: RII3-CT-2003-505925, by the Dubna JINR 07-04-1069-09/2011 project and by the VEGA 1/0295/08 (PB) and 1/0292/09 (DU) grants. The research leading to these results has received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agreement no. 226716 (HASYLAB project I-20080187 EC) to DU.

Author information

Authors and Affiliations

  1. Department of Physical Chemistry of Drugs, Faculty of Pharmacy, Comenius University, 832 32, Bratislava, Slovakia

    Jana Gallová, Daniela Uhríková, Norbert Kučerka, Slavomíra Doktorovová & Pavol Balgavý

  2. Canadian Neutron Beam Centre, National Research Council, Chalk River, Ontario, K0J 1P0, Canada

    Norbert Kučerka

  3. HASYLAB at DESY, 22603, Hamburg, Germany

    Sérgio S. Funari

  4. Laboratoire Léon Brillouin (CEA-CNRS), CEA Saclay, 91191, Gif Sur Yvette Cedex, France

    José Teixeira

Authors
  1. Jana Gallová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniela Uhríková
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Norbert Kučerka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Slavomíra Doktorovová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sérgio S. Funari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. José Teixeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pavol Balgavý
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jana Gallová.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gallová, J., Uhríková, D., Kučerka, N. et al. The effects of cholesterol and β-sitosterol on the structure of saturated diacylphosphatidylcholine bilayers. Eur Biophys J 40, 153–163 (2011). https://doi.org/10.1007/s00249-010-0635-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-010-0635-6

Keywords

Search

Navigation