Direct visualization of dispersed lipid bicontinuous cubic phases by cryo-electron tomography

Nature Communications

Volumn 6, Issue , 2015, Pages

  Demurtas, Davide ^a   Guichard, Paul ^a   Martiel, Isabelle ^b   Mezzenga, Raffaele ^b,d   Hébert, Cécile ^a   Sagalowicz, Laurent ^c  

^a EPFL   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c NESTLÉ RESEARCH CENTER   (Switzerland)

^d PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; LIPID BILAYER; MONOACYLGLYCEROL; WATER;

AQUEOUS SOLUTION; CELLS AND CELL COMPONENTS; LIPID; TOMOGRAPHY; TRANSPORT PROCESS;

AQUEOUS SOLUTION; ARTICLE; CRYOELECTRON MICROSCOPY; DISPERSION; ELECTRON TOMOGRAPHY; FOURIER TRANSFORMATION; LIPID ANALYSIS; LIPID BILAYER; LIQUID CRYSTAL; MATHEMATICAL MODEL; MEMBRANE FUSION; RADIATION SCATTERING; SIMULATION; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY; SMALL ANGLE SCATTERING; ULTRASTRUCTURE;

CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; IMAGING, THREE-DIMENSIONAL; LIPID BILAYERS; LIPIDS; LIQUID CRYSTALS; MONOGLYCERIDES; SCATTERING, SMALL ANGLE; WATER;

EID: 84947209760     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9915     Document Type: Article

References (46)

1. Luzzati, V., Tardieu, A. & Gulikkrz, T. Polymorphisms of lipids. Nature 217, 1028-1030 (1968).
2. Hyde, S. T., Andersson, S., Ericsson, B. & Larsson, K. A cubic structure consisting of a lipidic bilayer forming an infinite periodic minimum surface of the gyroid type in the glycerolmonoleat-water system. Z. Kristallogr. Cryst. Mater. 168, 213-220 (1984).
3. Salentinig, S., Phan, S., Khan, J., Hawley, A. & Boyd, B. J. Formation of highly organized nanostructures during the digestion of milk. ACS Nano 7, 10904-10911 (2013).
4. Sagalowicz, L. & Leser, M. E. Delivery systems for liquid food products. Curr. Opin. Colloid Interface Sci. 15, 61-72 (2010).
5. Almsherqi, Z. A., Kohlwein, S. D. & Deng, Y. Cubic membranes: a legend beyond the Flatland of cell membrane organization. J Cell Biol. 173, 839-844 (2006).
6. Tenchov, B., MacDonald, R. C. & Siegel, D. P. Cubic phases in phosphatidylcholine-cholesterol mixtures: cholesterol as membrane 'fusogen'. Biophys. J. 91, 2508-2516 (2006).
7. Mezzenga, R., Schurtenberger, P., Burbidge, A. & Michel, M. Understanding foods as soft materials. Nat. Mater. 4, 729-740 (2005).
8. Deng, Y. & Mieczkowski, M. Three-dimensional periodic cubic membrane structure in the mitochondria of amoebae Chaos carolinensis. Protoplasma 203, 16-25 (1998).
9. Leikin, S. L., Kozolv, M. M., Chernomordik, L. V., Markin, V. S. & Chizmadzhev, Y. A. Membrane-fusion - overcoming of the hydration barrier and local restructuring. J. Theor. Biol. 129, 411-425 (1987).
10. Porter, C. J. H., Revaskis, N. H. & Charman, W. N. Lipids and lipid-based formulations: optimizing the oral delivery of lipophilic drugs. Nat. Rev. 6, 231-248 (2007).
11. 2-adrenergic g protein-coupled receptor. Science 318, 1258-1265 (2007).
12. Zabara, A., Negrini, R., Onaca-Fischer, O. & Mezzenga, R. Perforated bicontinuous cubic phases with pH-responsive topological channel interconnectivity. Small 9, 3602-3621 (2013).
13. Sagalowicz, L. et al. Crystallography of dispersed liquid crystalline phase studies by cryo-transmission electron microscopy. J. Microsc. 221, 110-121 (2006).
14. Lucic, V., Forster, F. & Baumeister, W. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 74, 833-865 (2005).
15. Löbling, T. I. et al. Hidden structural features of multicompartment micelles revealed by cryogenic transmission electron tomography. ACS Nano 8, 11330-11340 (2014).
16. Berlepsch, H. V., Böttcher, C., Skrabania, K. & Laschewsky, A. Complex domain architecture of multicompartment micelles from a linear ABC triblock copolymer revealed by cryogenic electron tomography. Chem. Commun. 2290-2292 (2009).
17. Parry, A. L., Bomans, P. H., Holder, S. J., Sommerdijk, N. A. & Biagini, S. C. Cryo electron tomography reveals confined complex morphologies of tripeptide-containing amphiphilic double-comb diblock copolymers. Angew. Chem. Int. Ed. Engl. 47, 8859-8862 (2008).
18. Sali, A., Glaeser, R., Earnest, T. & Baumeister, W. From words to literature in structural proteomics. Nature 422, 216-225 (2003).
19. Gustafsson, M., Ljusberg-Wharen, H., Almgren, M. & Larsson, K. Submicron Particles of reversed lipid phases in water stabilized by a nonionic amphiphilic polymer. Langmuir. 13, 6964-6971 (1997).
20. Ishikawa, T., Sakakibara, H. & Oiwa, K. The architecture of outer dynein arms in situ. J. Mol. Biol. 368, 1249-1258 (2007).
21. Larsson, K. Cubic lipid-water phases: structures and biomembrane aspects. J. Phys. Chem. 93, 7304-7314 (1989).
22. von Schnering, H. G. & Nesper, R. Nodal surface of Fourier series: fundamental invariants of structured matter. Z. Phys. B Condens. Matter 83, 407-412 (1991).
23. Jacob, M., Larsson, K. & Andersson, S. Lipid bilayer standing wave conformation in aqueous cubic phases. Z. Kristallogr. 212, 5-8 (1997).
24. Andersson, S., Jacob, M. & Lidin, S. Structure of the cubosome-a closed lipid bilayer aggregate. Z. Kristallogr. 210, 315-318 (1995).
25. Angelov, B. et al. Detailed structure of diamond-type lipid cubic nanoparticles. J. Am. Chem. Soc. 128, 5813-5817 (2006).
26. Boyd, B. J., Rizwan, S. B., Dong, Y.-D., Hook, S. & Rades, T. Self-assembled geometric liquid-crystalline nanoparticles imaged in three dimensions: Hexosomes are not necessarily flat hexagonal prisms. Langmuir. 23, 12461-12464 (2007).
27. Mulet, X., Gong, X., Waddington, L. J. & Drummond, D. J. Observing Self-Assembled Lipid Nanoparticles Building Order and Complexity through Low-Energy Transformation Processes. ACS Nano 3, 2789-2797 (2009).
28. L cubic mesophase and its soft nanoparticles. Langmuir. 25, 1316-1326 (2009).
29. Siegel, D. P. Inverted micellar intermediates and the transitions between lamellar, cubic, and inverted hexagonal amphiphile phases III. Isotropic and inverted cubic state formation via intermediates in transitions between Lα and phases HII. Chem. Phys. Lipids 42, 279-301 (1986).
30. Yang, L. & Huang, H. V. Observation of a membrane fusion intermediate structure. Science 297, 1877-1879 (2002).
31. Arslan, I., Tong, J. R. & Midgley, P. A. Reducing the missing wedge: High-resolution dual axis tomography of inorganic materials. Ultramicroscopy 106, 994-1000 (2006).
32. Sagalowicz, L. et al. Influence of vitamin E acetate and other lipids on the phase behavior of mesophases based on unsaturated monoglycerides. Langmuir. 29, 8222-8232 (2013).
33. Spicer, P. T. et al. Novel process for producing cubic liquid crystalline nanoparticles (cubosomes). Langmuir. 17, 5748-5756 (2001).
34. Martiel, I., Sagalowicz, L., Handschin, S. & Mezzenga, R. Facile dispersion and control of internal structure in lyotropic liquid crystalline particles by auxiliary solvent evaporation. Langmuir. 30, 14452-14459 (2014).
35. Chong, J. Y. T., Mulet, X., Waddington, L. J., Boyd, B. J. & Drummond, C. J. High-throughput discovery of novel steric stabilizers for cubic lyotropic liquid crystal nanoparticle dispersions. Langmuir. 28, 9223-9232 (2012).
36. Johnsson, M., Barauskas, J. & Tiberg, F. Cubic phases and cubic phase dispersions in a phospholipid-based system. J. Am. Chem. Soc. 127, 1076-1077 (2005).
37. Barauskas, J., Johnsson, M., Joabsson, F. & Tiberg, F. Cubic phase nanoparticles (cubosomes): principles for controlling size, structure and stability. Langmuir. 21, 2569-2577 (2005).
38. La, Y. et al. Colloidal inverse bicontinuous cubic membranes of block copolymers with tunable surface functional groups. Nat. Chem. 6, 534-541 (2014).
39. De Campo, L. et al. Reversible phase transitions in emulsified nanostrutture lipid system. Langmuir. 20, 5254-5261 (2004).
40. Landh, T. Phase behavior in the system pine needle oil monoglycerides-poloxamer 407-water at 20.degree. J. Phys. Chem. 98, 8453-8467 (1994).
41. Martiel, I. et al. Oil and drug control the release rate from lyotropic liquid crystals. J. Control Release 204, 78-84 (2015).
42. Mastronarde, D. N. Dual-axis tomography: an approach with alignment methods that preserve resolution. J. Struct. Biol. 120, 343-352 (1997).
43. Messaoudi, C., Boudier, T., Sorzano, C. O. & Marco, S. TomoJ: tomography software for three-dimensional reconstruction in transmission electron microscopy. BMC Bioinformatics 8, 288 (2007).
44. Heymann, J. B. & Belnap, D. M. Bsoft: image processing and molecular modeling for electron microscopy. J. Struct. Biol. 157, 3-18 (2007).
45. Abramoff, M. D., Magalhaes, P. J. & Ram, S. J. Image processing with ImageJ. Biophoton. Int. 11, 36-42 (2004).
46. Pettersen, E. F. et al. UCSF Chimera a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).