Skip to main content
Log in

Effects of N,N-dimethyl-N-alkylamine-N-oxides on DOPC bilayers in unilamellar vesicles: small-angle neutron scattering study

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

Abstract

Small-angle neutron scattering data were collected from aqueous dispersions of unilamellar vesicles (ULVs) consisting of mixtures of 1,2-dioleoyl-sn-glycero-3-phosphatidylcholine and a homologous series of N,N-dimethyl-N-alkylamine-N-oxides (CnNO, n = 12, 14, 16, and 18, where n is the number of carbon atoms in the alkyl chain). A modeling approach was applied to the neutron scattering curves to obtain the bilayer structural parameters. Particularly, the external 2H2O/H2O contrast variation technique was carried out on pure dioleoylphosphatidylcholine (DOPC) ULVs to determine the hydrophilic region thickness \( D_{\text{h}} \) = 9.8 ± 0.6 Å. Consequently, the hydrocarbon region thickness \( 2D_{\text{C}} \), the lateral bilayer area per one lipid molecule \( A \), and the number of water molecules located in the hydrophilic region per one lipid molecule \( N_{\text{W}} \) were obtained from single-contrast neutron scattering curves using the previously determined \( D_{\text{h}} \). The structural parameters were extracted as functions of \( r_{{{\text{C}}n{\text{NO}}}} \) (the CnNO:DOPC molar ratio) and n. The dependences \( A(r_{{{\text{C}}n{\text{NO}}}} ) \) provided the partial lateral areas of CnNOs (\( \bar{A}_{{{\text{C}}n{\text{NO}}}} \)) and DOPC (\( \bar{A}_{\text{DOPC}} \)) in bilayers. It was observed that the \( \bar{A}_{{{\text{C}}n{\text{NO}}}} \)’s were constant in the investigated interval of \( r_{{{\text{C}}n{\text{NO}}}} \) and for n = 12, 14, and 16 equal to 36.6 ± 0.4 Å2, while \( \bar{A}_{{{\text{C}}18{\text{NO}}}} \) increased to 39.4 ± 0.4 Å2. The bilayer hydrocarbon region thickness \( 2D_{\text{C}} \) decreased with intercalation of each CnNO. This effect increased with \( r_{{{\text{C}}n{\text{NO}}}} \) and decreased with increasing CnNO alkyl chain length. The intercalation of C18NO changed the \( 2D_{\text{C}} \) only slightly. To quantify the effect of CnNO intercalation into DOPC bilayers we fit the \( 2D_{\text{C}} (r_{{{\text{C}}n{\text{NO}}}} ) \) dependences with weighted linear approximations and acquired their slopes \( \Delta d \).

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Balgavý P, Devínsky F (1996) Cut-off effects in biological activities of surfactants. Adv Colloid Int Sci 66:23–63. doi:10.1016/0001-8686(96)00295-3

    Article  Google Scholar 

  • Balgavý P, Uhríková D, Gallová J, Lohner K, Degovics G (1993) Interaction of tertiary amine anesthetics with phosphatidylcholine bilayers. In: Laggner P, Glatter O (eds) Trends in colloid interface science VII. Steinkopff, Germany, pp 184–185. doi:10.1007/BFb0118503

  • Balgavý P, Kučerka N, Gordeliy VI, Cherezov VG (2001) Evaluation of small-angle neutron scattering curves of unilamellar phosphatidylcholine liposomes using a multishell model of bilayer neutron scattering length density. Acta Phys Slovaca 51:53–68

    Google Scholar 

  • Barlow DJ, Lawrence MJ, Zuberi T, Zuberi S, Heenan RK (2000) Small-angle neutron-scattering studies on the nature of the incorporation of polar oils into aggregates of N,N-dimethyldodecylamine-N-oxide. Langmuir 16:10398–10403. doi:10.1021/la0002233

    Article  CAS  Google Scholar 

  • Belička M, Klacsová M, Karlovská J, Westh P, Devínsky F, Balgavý P (2014) Molecular and component volumes of N,N-dimethyl-N-alkylamine-N-oxides in DOPC bilayers. Chem Phys Lipids 180:1–6. doi:10.1016/j.chemphyslip.2014.02.007

    Google Scholar 

  • Benjamin L (1966) Partial molal volume changes during micellization and solution of nonionic surfactants and perfluorocarboxylates using a magnetic density balance. J Phys Chem 70:3790–3797. doi:10.1021/j100884a006

    Article  CAS  Google Scholar 

  • Búcsi A, Karlovská J, Chovan M, Devínsky F, Uhríková D (2014) Determination of pKa of N-alkyl-N,N-dimethylamine-N-oxides using 1H NMR and 13C NMR spectroscopy. Chem Pap 68:842–846. doi: 10.2478/s11696-013-0517-3

    Google Scholar 

  • Büldt G, Gally HU, Seelig J, Zaccai G (1979) Neutron diffraction studies on phosphatidylcholine model membranes: I. Head group conformation. J Mol Biol 134:673–691. doi:10.1016/0022-2836(79)90479-0

    Article  PubMed  Google Scholar 

  • Chang DL, Rosano HL, Woodward AE (1985) Carbon-13 NMR study of the effects of pH on dodecyldimethylamine oxide solutions. Langmuir 1:669–672. doi:10.1021/la00066a006

    Article  CAS  Google Scholar 

  • Devínsky F (1986) Amine oxides. XVII. Non-aromatic amine oxides: Their use in organic synthesis and industry. Acta Fac Pharm Univ Comen 40:63–83

    Google Scholar 

  • Devínsky F, Lacko I, Nagy A, Krasnec L (1978) Amine oxides. I. Synthesis, 1H-NMR, and infrared spectra of 4-alkylmorpholine-N-oxides. Chem Zvesti: Chem Pap 32:106–115

    Google Scholar 

  • Devínsky F, Kopecká-Leitmanová A, Šeršeň F, Balgavý P (1990) Cut-off effect in antimicrobial activity and in membrane perturbation efficiency of the homologous series of N,N-dimethylalkylamine oxides. J Pharm Pharmacol 42:790–794. doi:10.1111/j.2042-7158.1990.tb07022.x

    Article  PubMed  Google Scholar 

  • Dubničková M, Kiselev M, Kutuzov S, Devínsky F, Gordeliy V, Balgavý P (1997) Effect of N-lauryl-N, N-dimethylamine-N-oxide on dimyristoyl phosphatidylcholine bilayer thickness: a small-angle neutron scattering study. Gen Physiol Biophys 16:175

    PubMed  Google Scholar 

  • Egelhaaf SU, Wehrli E, Müller M, Adrian M, Schurtenberger P (1996) Determination of the size distribution of lecithin liposomes: a comparative study using freeze fracture, cryoelectron microscopy and dynamic light scattering. J Microsc 184:214–228. doi:10.1046/j.1365-2818.1996.1280687.x

    Article  CAS  Google Scholar 

  • Garamus V, Kameyama K, Kakehashi R, Maeda H (1999) Neutron scattering and electrophoresis of dodecyldimethylamine oxide micelles. Colloid Polym Sci 277:868–874. doi:10.1007/s003960050463

    Article  CAS  Google Scholar 

  • Glover RE, Smith RR, Jones MV, Jackson SK, Rowlands CC (1999) An EPR investigation of surfactant action on bacterial membranes. FEMS Microbiol Lett 177:57–62. doi:10.1111/j.1574-6968.1999.tb13713.x

    Article  PubMed  CAS  Google Scholar 

  • Gorski N, Gradzielski M, Hoffmann H (1994) Mixtures of nonionic and ionic surfactants. The effect of counterion binding in mixtures of tetradecyldimethylamine oxide and tetradecyltrimethylammonium bromide. Langmuir 10:2594–2603. doi:10.1021/la00020a018

    Article  CAS  Google Scholar 

  • Heberle FA, Pan J, Standaert RF, Drazba P, Kučerka N, Katsaras J (2012) Model-based approaches for the determination of lipid bilayer structure from small-angle neutron and X-ray scattering data. Eur Biophys J 41:875–890. doi:10.1007/s00249-012-0817-5

    Article  PubMed  CAS  Google Scholar 

  • Herrmann KW (1962) Non-ionic—cationic micellar properties of dimethylamine oxide. J Phys Chem 66:295–300. doi:10.1021/j100808a025

    Article  CAS  Google Scholar 

  • Hunter DG, Frisken BJ (1998) Effect of extrusion pressure and lipid properties on the size and polydispersity of lipid vesicles. Biophys J 74:2996–3002. doi:10.1016/S0006-3495(98)78006-3

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Huster D, Jin AJ, Arnold K, Gawrisch K (1997) Water permeability of polyunsaturated lipid membranes measured by 17O NMR. Biophys J 73:855–864. doi:10.1016/S0006-3495(97)78118-9

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jahnová E, Ferenčík M, Nyulassy Š, Devínsky F, Lacko I (1993) Amphiphilic detergents inhibit production of IgG and IgM by human peripheral blood mononuclear cells. Immunol Lett 39:71–75. doi:10.1016/0165-2478(93)90166-Y

    Article  PubMed  Google Scholar 

  • Karlovská J, Lohner K, Degovics G, Lacko I, Devı́nsky F, Balgavý P (2004) Effects of non-ionic surfactants N-alkyl-N,N-dimethylamine-N-oxides on the structure of a phospholipid bilayer: small-angle X-ray diffraction study. Chem Phys Lipids 129:31–41. doi:10.1016/j.chemphyslip.2003.11.003

    Article  PubMed  CAS  Google Scholar 

  • Karlovská J, Uhríková D, Kučerka N, Teixeira J, Devínsky F, Lacko I, Balgavý P (2006) Influence of N-dodecyl-N,N-dimethylamine N-oxide on the activity of sarcoplasmic reticulum Ca2+-transporting ATPase reconstituted into diacylphosphatidylcholine vesicles: effects of bilayer physical parameters. Biophys Chem 119:69–77. doi:10.1016/j.bpc.2005.09.007

    Article  PubMed  CAS  Google Scholar 

  • Kiselev MA, Lombardo D, Kisselev AM, Lesieur P, Aksenov VL (2003) Structure factor of dimyristoylphosphatidylcholine unilamellar vesicles: small-angle X-ray scattering study. Poverhnost 11:20–24

    Google Scholar 

  • Klacsová M, Bulacu M, Kučerka N, Uhríková D, Teixeira J, Marrink SJ, Balgavý P (2011) The effect of aliphatic alcohols on fluid bilayers in unilamellar DOPC vesicles—a small-angle neutron scattering and molecular dynamics study. Biochim Biophys Acta 1808:2136–2146. doi:10.1016/j.bbamem.2011.04.010

    Article  PubMed  CAS  Google Scholar 

  • Kotlarchyk M, Huang JS, Chen SH (1985) Structure of AOT reversed micelles determined by small-angle neutron scattering. J Phys Chem 89:4382–4386. doi:10.1021/j100266a046

    Article  CAS  Google Scholar 

  • Kučerka N, Kiselev MA, Balgavý P (2004a) 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. doi:10.1007/s00249-003-0349-0

    Article  PubMed  CAS  Google Scholar 

  • Kučerka N, Nagle JF, Feller SE, Balgavý P (2004b) Models to analyze small-angle neutron scattering from unilamellar lipid vesicles. Phys Rev E 69:051903. doi:10.1103/PhysRevE.69.051903

    Article  CAS  Google Scholar 

  • Kučerka N, Pencer J, Sachs JN, Nagle JF, Katsaras J (2007) Curvature effect on the structure of phospholipid bilayers. Langmuir 23:1292–1299. doi:10.1021/la062455t

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kučerka N, Nagle JF, Sachs JN, Feller SE, Pencer J, Jackson A, Katsaras J (2008) Lipid bilayer structure determined by the simultaneous analysis of neutron and X-ray scattering data. Biophys J 95:2356–2367. doi:10.1529/biophysj.108.132662

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kučerka N, Gallová J, Uhríková D, Balgavý P, Bulacu M, Marrink S-J, Katsaras J (2009) Areas of monounsaturated diacylphosphatidylcholines. Biophys J 97:1926–1932. doi:10.1016/j.bpj.2009.06.050

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kuklin AI, Islamov AK, Gordeliy VI (2005) Two-detector system for small-angle neutron scattering instrument. Neutron News 16:16–18. doi:10.1080/10448630500454361

    Article  Google Scholar 

  • Kuklin AI, Islamov AK, Kovalev YS, Utrobin PK, Gordeliy VI (2006) Optimization two-detector system small-angle neutron spectrometer YuMO for nanoobject investigation. J Surf Invest X-Ray Synchrotron Neutron Tech 6:74–83

    Google Scholar 

  • Kuklin AI, Kovalev YC, Ivankov AI, Soloviev DV, Rogachev AV, Soloviev AG, Utrobin PK, Gordeliy VI (2013) Some specific features of experiment realization at SANS spectrometer at IBR-2. In: Communication P14-2013-46 of the Joint Institute for Nuclear Research, Dubna. http://www1.jinr.ru/Preprints/2013/046(P14-2013-46).pdf

  • Lide DR (2004) CRC handbook of chemistry and physics 2004–2005: a ready-reference book of chemical and physical data. CRC Press, Boca Raton

    Google Scholar 

  • Lorenz CD, Hsieh C-M, Dreiss CA, Lawrence MJ (2011) Molecular dynamics simulations of the interfacial and structural properties of dimethyldodecylamine-N-oxide micelles. Langmuir 27:546–553. doi:10.1021/la1031416

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • MacDonald RC, MacDonald RI, Menco BPM, Takeshita K, Subbarao NK, Hu L (1991) Small-volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim Biophys Acta 1061:297–303. doi:10.1016/0005-2736(91)90295-J

    Article  PubMed  CAS  Google Scholar 

  • Maeda H, Tanaka S, Ono Y, Miyahara M, Kawasaki H, Nemoto N, Almgren M (2006) Reversible micelle-vesicle conversion of oleyldimethylamine oxide by pH changes. J Phys Chem B 110:12451–12458. doi:10.1021/jp056967c

    Article  PubMed  CAS  Google Scholar 

  • Murín A, Devínsky F, Koleková A, Lacko I (1990) Relation between chemical structure and biological activity of N-alkyl dimethylaminoxides series and some other related components. Biologia (Bratislava) 45:521–531

    Google Scholar 

  • Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta 1469:159–195. doi:10.1016/S0304-4157(00)00016-2

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nawroth T, Conrad H, Dose K (1989) Neutron small angle scattering of liposomes in the presence of detergents. Phys B 156–157:477–480. doi:10.1016/0921-4526(89)90708-4

    Article  Google Scholar 

  • Ostanevich YM (1988) Time-of-flight small-angle scattering spectrometers on pulsed neutron sources. Macromol Symp 15:91–103. doi:10.1002/masy.19880150107

    Article  Google Scholar 

  • Pabst G, Rappolt M, Amenitsch H, Laggner P (2000) Structural information from multilamellar liposomes at full hydration: full q-range fitting with high quality X-ray data. Phys Rev E 62:4000–4009. doi:10.1103/PhysRevE.62.4000

    Article  CAS  Google Scholar 

  • Pan J, Tristram-Nagle S, Kučerka N, Nagle JF (2008) Temperature dependence of structure, bending rigidity, and bilayer interactions of dioleoylphosphatidylcholine bilayers. Biophys J 94:117–124. doi:10.1529/biophysj.107.115691

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pedersen JS (1993) Resolution effects and analysis of small-angle neutron scattering data. J Phys IV Fr 3:C8–C491. doi:10.1051/jp4:19938102

    Article  Google Scholar 

  • Pedersen JS, Svaneborg C, Almdal K, Hamley IW, Young RN (2003) A small-angle neutron and X-ray contrast variation scattering study of the structure of block copolymer micelles: corona shape and excluded volume interactions. Macromolecules 36:416–433. doi:10.1021/ma0204913

    Article  CAS  Google Scholar 

  • Sadler DM, Reiss-Husson F, Rivas E (1990) Thickness measurements of single walled dimyristoyl phosphatidylcholine vesicles by neutron scattering. Chem Phys Lipids 52:41–48. doi:10.1016/0009-3084(90)90005-C

    Article  PubMed  CAS  Google Scholar 

  • Sears VF (1992) Neutron scattering lengths and cross sections. Neutron News 3:26–37. doi:10.1080/10448639208218770

    Article  Google Scholar 

  • Šeršeň F, Leitmanová A, Devínsky F, Lacko I, Balgavỳ P (1989) A spin label study of perturbation effects of N-(1-methyldodecyl)-N,N,N-trimethylammonium bromide and N-(1-methyldodecyl)-N,N-dimethylamine oxide on model membranes prepared from Escherichia coli-isolated lipids. Gen Physiol Biophys 8:133–156

    PubMed  Google Scholar 

  • Šeršeň F, Balgavý P, Devínsky F (1990) Electron spin resonance study of chloroplast photosynthetic activity in the presence of amphiphilic amines. Gen Physiol Biophys 9:625–633

    PubMed  Google Scholar 

  • Šeršeň F, Gabunia G, Krejčířová E, Kráľová K (1992) The relationship between lipophilicity of N-alkyl-N,N-dimethylamine oxides and their effects on the thylakoid membranes of chloroplasts. Photosynthetica 26:205–212

    Google Scholar 

  • Soloviev AG, Litvinenko EI, Ososkov GA, Islamov AK, Kuklin AI (2003) Application of wavelet analysis to data treatment for small-angle neutron scattering. Nucl Instrum Methods Phys Res Sect A 502:500–502. doi:10.1016/S0168-9002(03)00481-9

    Article  CAS  Google Scholar 

  • Sun W-J, Suter RM, Knewtson MA, Worthington CR, Tristram-Nagle S, Zhang R, Nagle JF (1994) Order and disorder in fully hydrated unoriented bilayers of gel-phase dipalmitoylphosphatidylcholine. Phys Rev E 49:4665–4676. doi:10.1103/PhysRevE.49.4665

    Article  CAS  Google Scholar 

  • Tanford C (1980) The hydrophobic effect, 2nd edn. Wiley, New York

    Google Scholar 

  • Tristram-Nagle S, Liu Y, Legleiter J, Nagle JF (2002) Structure of gel phase DMPC determined by X-ray diffraction. Biophys J 83:3324–3335. doi:10.1016/S0006-3495(02)75333-2

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Uhríková D, Kučerka N, Islamov A, Gordeliy V, Balgavý P (2001) Small-angle neutron scattering study of N-dodecyl-N,N-dimethylamine N-oxide induced solubilization of dioleoylphosphatidylcholine bilayers in liposomes. Gen Physiol Biophys 20:183–189

    PubMed  Google Scholar 

  • Uhríková D, Rybár P, Hianik T, Balgavý P (2007) Component volumes of unsaturated phosphatidylcholines in fluid bilayers: a densitometric study. Chem Phys Lipids 145:97–105. doi:10.1016/j.chemphyslip.2006.11.004

    Article  PubMed  CAS  Google Scholar 

  • Zaccai G, Büldt G, Seelig A, Seelig J (1979) Neutron diffraction studies on phosphatidylcholine model membranes: II. Chain conformation and segmental disorder. J Mol Biol 134:693–706. doi:10.1016/0022-2836(79)90480-7

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by JINR project 04-4-1069-2009/2014, by the VEGA 1/0159/11 and 1/1224/12 grants, and by the APVV-0212-10 grant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michal Belička.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 542 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Belička, M., Kučerka, N., Uhríková, D. et al. Effects of N,N-dimethyl-N-alkylamine-N-oxides on DOPC bilayers in unilamellar vesicles: small-angle neutron scattering study. Eur Biophys J 43, 179–189 (2014). https://doi.org/10.1007/s00249-014-0954-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-014-0954-0

Keywords

Navigation