Hepatitis B subvirus particles display both a fluid bilayer membrane and a strong resistance to freeze drying: A study by solid-state NMR, light scattering, and cryo-electron microscopy/tomography

FASEB Journal

Volumn 27, Issue 10, 2013, Pages 4316-4326

  Grélard, Axelle ^a,b   Guichard, Paul ^c,d   Bonnafous, Pierre ^a,b   Marco, Sergio ^c,d   Lambert, Olivier ^a,b   Manin, Catherine ^e   Ronzon, Frédéric ^e   Dufourc, Erick J ^a,b,c  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b CNRS   (France)

^c INSTITUT CURIE   (France)

^d INSERM   (France)

^e SANOFI PASTEUR   (France)

Author keywords

Deuterium labeling; Lipid incorporation; Lipid thickness; Order parameter; Trapped water

Indexed keywords

DEUTERIUM; HEPATITIS B SURFACE ANTIGEN; PHOSPHOLIPID;

ARTICLE; BILAYER MEMBRANE; CRYOELECTRON MICROSCOPY; FREEZE DRYING; HEPATITIS B VIRUS; LIGHT SCATTERING; LIPID BILAYER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; SOLID STATE; TOMOGRAPHY; VIRUS PARTICLE; CELL MEMBRANE; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PICHIA;

CELL MEMBRANE; CRYOELECTRON MICROSCOPY; FREEZE DRYING; HEPATITIS B SURFACE ANTIGENS; MAGNETIC RESONANCE SPECTROSCOPY; PICHIA;

EID: 84885130995     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-232843     Document Type: Article

References (65)

1. Gilbert, R. J. C., Beales, L., Blond, D., Simon, M. N., Chisari, F. V., Stuart, D. I., and Rowlands, D. J. (2005) Hepatitis B small surface antigen particles are octahedral. Proc. Natl. Acad. Sci. U. S. A. 102, 14783-14788
2. McAleer, W. J., Buynak, E. B., Maigetter, R. Z., Wampler, D. E., and Hilleman, M. R (1984) Human hepatitis-B vaccine from recombinant yeast. Nature 307, 178-180
3. Gastaminza, P., Dryden, K. A., Boyd, B., Wood, M. R, Law, M., and Chisari, F. V. (2010) Ultrastructural and biophysical characterization of hepatitis C virus particles produced in cell culture. J. Virol. 84, 10999-11009
4. Hernandez, L. D., Hoffman, L. R, Wolfsberg, T. G, and White, J. M. (1996) Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12, 627-661
5. Kang, S. M., Song, J. M., Quan, F. S., and Compans, R. W. (2009) Influenza vaccines based on virus-like particles. Virus Res. 143, 140-146
6. Milhiet, P. E., Dosset, P., Godefroy, C., Le Grimellec, C., Larquet, E., Ronzon, F., and Manin, C. (2011) Nanoscale topography of hepatitis B antigen particles by atomic force microscopy. Biochimie (Paris) 93, 254-259
7. Greiner, V. J., Egele, C., Oncul, S., Ronzon, F., Klymchenko, A., and Mely, Y. (2010) Characterization of the lipid and protein organization in HBsAg viral particles by steady-state and time-resolved fluorescence spectroscopy. Biochimie (Paris) 92, 994-1002
8. Satoh, O., Imai, H., Yoneyama, T., Miyamura, T., Inoue, K., and Umeda, M. (2000) Membrane structure of the hepatitis B virus surface antigen particle. J. Biochem. 127, 543-550
9. Bothorel, P., and Lussan, C. (1968) Model of biological membrane based on lipid-protein interactions. C. R. Hebd. Seances Acad. Sci. D 266, 2492-2494
10. Singer, S. J., and Nicolson, G. L. (1972) The fluid mosaic model of the structure of cell membranes. Science 175, 720-731
11. Veldhuizen, R., Nag, K., Orgeig, S., and Possmayer, F. (1998) The role of lipids in pulmonary surfactant. Biochim. Biophys. Acta-Mol. Basis Dis. 1408, 90-108
12. Cullis, P. R., and Dekruijff, B. (1979) Lipid polymorphism and the functional roles of lipids in biological-membranes. Biochim. Biophys. Acta 559, 399-420
13. Cullis, P. R., and Hope, M. J. (1978) Effects of fusogenic agent on membrane structure of erythrocyte-ghosts and mechanism of membrane-fusion. Nature 271, 672-674
14. Derossi, D., Chassaing, G., and Prochiantz, A. (1998) Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 8, 84-87
15. Schmitz, G., and Muller, G. (1991) Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. J. Lipid Res. 32, 1539-1570
16. Israelachvili, J. N., Mitchell, D. J., and Ninham, B. W. (1977) Theory of self-assembly of lipid bilayers and vesicles. Biochim. Biophys. Acta 470, 185-201
17. Larijani, B., and Dufourc, E. J. (2006) Polyunsaturated phosphatidylinositol and diacylglycerol substantially modify the fluidity and polymorphism of biomembranes: a solid-state deuterium NMR study. Lipids 41, 925-932
18. Cevc, G. (1993) Phospholipids Handbook, Marcel Dekker, New York
19. Aussenac, F., Laguerre, M., Schmitter, J. M., and Dufourc, E. J. (2003) Detailed structure and dynamics of bicelle phospholipids using selectively deuterated and perdeuterated labels. H-2 NMR and molecular mechanics study. Langmuir 19, 10468-10479
20. Raffard, G., Steinbruckner, S., Arnold, A., Davis, J. H., and Dufourc, E. J. (2000) Temperature-composition diagram of dimyristoyl-dicaproyl phosphatidylcholine "bicelles " self-orienting in the magnetic field. A solid state 2H and 31P-NMR study. Langmuir 16, 7655-7662
21. Bechinger, B. (1999) The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta Biomembr. 1462, 157-183
22. Marassi, F. M., Ma, C., Gratkowski, H., Straus, S. K., Oblatt-Montal, M., Montal, M., and Opella, S. J. (1999) Correlation of the structural and functional domains in the membrane protein Vpu from HIV-1. Proc. Natl. Acad. Sci. U. S. A. 96, 14336-14341
23. Park, S. H., Loudet, C., Marassi, F. M., Dufourc, E. J., and Opella, S. J. (2008) Solid-state NMR spectroscopy of a membrane protein in biphenyl phospholipid bicelles with the bilayer normal parallel to the magnetic field. J. Magn. Reson. 193, 133-138
24. Davis, J. H. (1983) The description of membrane lipid conformation, order and dynamics by H-2-NMR. Biochim. Biophys. Acta 737, 117-171
25. Dufourc, E. J. (2008) Sterols and membrane dynamics. J. Chem. Biol. 1, 63-77
26. Dufourc, E. J. (2009) NMR for lipids and biomembranes. In Wiley Encyclopedia of Chemical Biology p. wecb 389, John Wiley & Sons, Chichester, UK
27. Grelard, A., Couvreux, A., Loudet, C., and Dufourc, E. J. (2009) Solution and solid state NMR of lipids. In Methods in Molecular Biology: Lipid Signaling Protocols (Larijani, B., Woscholski, R., and Rosser, C. A., eds) Vol. 462, pp. 111-133, Humana Press (Springer), Totowa, NJ, USA
28. Seelig, J. (1977) Deuterium magnetic resonance: theory and application to lipid membranes. Q. Rev. Biophys. 10, 353-418
29. Gamier-Lhomme, M., Grelard, A., Byrne, R. D., Loudet, C., and Larijani, B. (2007) Probing the dynamics of intact cells and nuclear envelope precursor membrane vesicles by deuterium solid state NMR spectroscopy. Biochim. Biophys. Acta Biomembr. 1768, 2516-2527
30. Petersen, N. O., and Chan, S. I. (1977) More on motional state of lipid bilayer membranes-interpretation of order parameters obtained from nuclear magnetic-resonance experiments. Biochemistry 16, 2657-2667
31. Schindler, H., and Seelig, J. (1975) Deuterium order parameters in relation to thermodynamic properties of a phospholipid bilayer-statistical mechanical interpretation. Biochemistry 14, 2283-2287
32. Douliez, J. P., Bechinger, B., Davis, J. H., and Dufourc, E. J. (1996) C-C bond order parameters from H-2 and C-13 solidstate NMR. J. Phys. Chem. 100, 17083-17086
33. Douliez, J. P., Ferrarini, A., and Dufourc, E. J. (1998) On the relationship between C-C and C-D order parameters and its use for studying the conformation of lipid acyl chains in biomembranes. J. Chem. Phys. 109, 2513-2518
34. Douliez, J. P., Leonard, A., and Dufourc, E. J. (1995) Restatement of order parameters in biomembranes-calculation of c-c bond order parameters from c-d quadrupolar splittings. Biophys. J. 68, 1727-1739
35. 14. J. Chem. Phys. 55, 5829-5831
36. Dufourc, E. J., Parish, E. J., Chitrakorn, S., and Smith, I. C. P. (1984) Structural and dynamical details of cholesterol lipid interaction as revealed by deuterium NMR. Biochemistry 23, 6062-6071
37. Leonard, A., and Dufourc, E. J. (1991) Interactions of cholesterol with the membrane lipid matrix-a solid-state NMR approach. Biochimie (Paris) 73, 1295-1302
38. Léonard, A., Milon, A., Krajewski-Bertrand, M.-A., and Dufourc, E. J. (1993) Modulation of membrane hydrophobic thickness by cholesterol, cycloartenol and hopanoid. a solid state 2H-NMR study. Bull. Magn. Reson. 15, 124-127
39. Garnier-Lhomme, M., Dufourc, E. J., Larijani, B., and Poccia, D. L. (2009) Lipid quantification and structure determination of nuclear envelope precursor membranes in the sea urchin. In Methods in Molecular Biology: Lipid Signaling Protocols (Larijani, B., Woscholski, R., and Rosser, C. A., eds), Vol. 462, pp. 89-110, Humana Press (Springer), Totowa, NJ, USA
40. Thurmond, R. L., Lindblom, G., and Brown, M. F. (1993) Curvature, order, and dynamics of lipid hexagonal phases studied by deuterium NMR spectroscopy. Biochemistry 32, 5394-5410
41. Meier, P., Sachse, J. H., Brophy, P. J., Marsh, D., and Kothe, G. (1987) Integral membrane proteins significantly decrease the molecular motion in lipid bilayers: a deuteron NMR relaxation study of membranes containing myelin proteolipid apoprotein. Proc. Natl. Acad. Sci. U. S. A. 84, 3704-3708
42. Diminsky, D., Schirmbeck, R., Reimann, J., and Barenholz, Y. (1997) Comparison between hepatitis B surface antigen (HBsAg) particles derived from mammalian cells (CHO) and yeast cells (Hansenula polymorpha): composition, structure, and immunogenicity. Vaccine 15, 637-647
43. Saxton, W. O., Baumeister, W., and Hahn, M. (1984) 3-Dimensional reconstruction of imperfect two-dimensional crystals. Ultramicroscopy 13, 57-70
44. Kremer, J. R., Mastronarde, D. N., and McIntosh, J. R. (1996) Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76
45. Messaoudil, C., Boudier, T., Sorzano, C. O. S., and Marco, S. (2007) TomoJ: tomography software for three-dimensional reconstruction in transmission electron microscopy. BMC Bioinformatics 8, 288
46. Herman, G. T., Lent, A., and Rowland, S. W. (1973) Artmathematics and applications-report on mathematical foundations and on applicability to real data of algebraic reconstruction techniques. J. Theor. Biol. 42, 1-32
47. Abramoff, M. D., Magalhães, P. J., and Ram, S. J. (2004) Image processing with ImageJ. Biophotonics Int. 11, 36-42
48. Davis, J. H., Jeffrey, K. R., Bloom, M., Valic, M. I., and Higgs, T. P. (1976) Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42, 390-394
49. Bloom, M., Davis, J. H., and Mackay, A. L. (1981) Direct determination of the oriented sample NMR spectrum from the powder spectrum for systems with a local axial symmetry. Chem. Phys. Lett. 80, 198-202
50. Sternin, E., Bloom, M., and MacKay, A. L. (1983) De-Pake-ing of NMR spectra. J. Magn. Reson. 55, 274-282
51. Buchoux, S., Lai-Kee-Him, J., Garnier, M., Tsan, P., Brisson, A., and Dufourc, E. J. (2008) Surfactin-triggered small vesicle formation of negatively charged membranes: A novel membrane-lysis mechanism. Biophys. J. 95, 3840-3849
52. Pott, T., and Dufourc, E. J. (1995) Action of melittin on the DPPC-cholesterol liquid-ordered phase-a solid-state h-2-nmr and p-31-nmr study. Biophys. J. 68, 965-977
53. Douliez, J. P., Leonard, A., and Dufourc, E. J. (1996) Conformational order of DMPC sn-1 versus sn-2 chains and membrane thickness: An approach to molecular protrusion by solid state H-2-NMR and neutron diffraction. J. Phys. Chem. 100, 18450-18457
54. Buldt, G., Gally, H. U., Seelig, J., and Zaccai, G. (1979) Neutron-diffraction studies on phosphatidylcholine model membranes. 1. Head group conformation. J. Mol. Biol. 134, 673-691
55. Tu, K., Tobias, D. J., Blasie, J. K., and Klein, M. L. (1996) Molecular dynamics investigation of the structure of a fully hydrated gel-phase dipalmitoylphosphatidylcholine bilayer. Biophys. J. 70, 595-608
56. Tu, K., Tobias, D. J., and Klein, M. L. (1995) Constant pressure and temperature molecular dynamics simulation of a fully hydrated liquid crystal phase dipalmitoylphosphatidylcholine bilayer. Biophys. J. 69, 2558-2562
57. Garnier, M., Dufourc, E. J., and Larijani, B. (2006) Characterisation of lipids in cell signalling and membrane dynamics by nuclear magnetic resonance spectroscopy and mass spectrometry. Signal Transduct. 6, 133-143
58. Garnier-Lhomme, M., Byrne, R. D., Hobday, T. M. C., Gschmeissner, S., Poccia, D. L., Dufourc, E. J., and Larijani, B. (2009) Nuclear envelope remnants: fluid membranes enriched in sterols and polyphosphoinositides. PLoS One 4, 12
59. Bothorel, P., Belle, J., and Lemaire, B. (1974) Theoretical study of aliphatic chain structure in monolayers and bilayers. Chem. Phys. Lipids 12, 96-116
60. Helfrich, W. (1973) Elastic properties of lipid bilayers-theory and possible experiments. Z. Naturforsch. C 28, 693-703
61. Deuling, H. J., and Helfrich, W. (1976) Curvature elasticity of fluid membranes-catalog of vesicle shapes. J. Physique 37, 1335-1345
62. Fernandez-Puente, L., Bivas, I., Mitov, M. D., and Méléard, P. (1994) Temperature and chain length effects on bending elasticity of phosphatidylcholine bilayers. Europhys. Lett. 28, 181-186
63. Maringer, K., Stylianou, J., and Elliott, G. (2012) A network of protein interactions around the Herpes simplex virus tegument protein VP22. J. Virol. 86, 12971-12982
64. Dichtelmuller, H., Rudnick, D., and Kloft, M. (2002) Inactivation of lipid enveloped viruses by octanoic acid treatment of immunoglobulin solution. Biologicals 30, 135-142
65. Roberts, K. L., Breiman, A., Carter, G. C., Ewles, H. A., Law, M., and Smith, G. L. (2009) Acidic residues in the membrane-proximal stalk region of vaccinia virus protein B5 are required for glycosaminoglycan-mediated disruption of the extracellular enveloped virus outer membrane. J. Gen. Virol. 90, 1582-1591