Influenza viral membrane fusion is sensitive to sterol concentration but surprisingly robust to sterol chemical identity

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Zawada, Katarzyna E ^a   Wrona, Dominik ^a,b   Rawle, Robert J ^a   Kasson, Peter M ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CYCLODEXTRIN DERIVATIVE; CHOLESTEROL; LIPOSOME; MEMBRANE LIPID; METHYL-BETA-CYCLODEXTRIN; STEROL; VIRUS HEMAGGLUTININ;

ANIMAL; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; DOG; INFLUENZA A VIRUS (H3N2); KINETICS; MDCK CELL LINE; MEMBRANE FUSION; METABOLISM; MOLECULAR DYNAMICS; ULTRASTRUCTURE; VIRION;

ANIMALS; BETA-CYCLODEXTRINS; CELL MEMBRANE; CHOLESTEROL; CRYOELECTRON MICROSCOPY; DOGS; HEMAGGLUTININS, VIRAL; INFLUENZA A VIRUS, H3N2 SUBTYPE; KINETICS; LIPOSOMES; MADIN DARBY CANINE KIDNEY CELLS; MEMBRANE FUSION; MEMBRANE LIPIDS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; STEROLS; VIRION;

EID: 84979031513     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep29842     Document Type: Article

References (42)

1. Gerl, M. J. et al. Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J Cell Biol 196, 213-221 (2012).
2. Haque, M. E., McIntosh, T. J., Lentz, B. R. Influence of lipid composition on physical properties and PEG-mediated fusion of curved and uncurved model membrane vesicles: "Nature's own" fusogenic lipid bilayer. Biochemistry 40, 4340-4348 (2001).
3. Lee, D. E., Lew, M. G., Woodbury, D. J. Vesicle fusion to planar membranes is enhanced by cholesterol and low temperature. Chem Phys Lipids 166, 45-54 (2013).
4. Biswas, S., Yin, S. R., Blank, P. S., Zimmerberg, J. Cholesterol promotes hemifusion and pore widening in membrane fusion induced by influenza hemagglutinin. J Gen Physiol 131, 503-513 (2008).
5. Razinkov, V. I., Cohen, F. S. Sterols and sphingolipids strongly affect the growth of fusion pores induced by the hemagglutinin of influenza virus. Biochemistry 39, 13462-13468 (2000).
6. Sun, X., Whittaker, G. R. Role for influenza virus envelope cholesterol in virus entry and infection. J Virol 77, 12543-12551 (2003).
7. Domanska, M. K., Wrona, D., Kasson, P. M. Multiphasic effects of cholesterol on influenza fusion kinetics reflect multiple mechanistic roles. Biophys J 105, 1383-1387 (2013).
8. Nussbaum, O., Rott, R., Loyter, A. Fusion of influenza virus particles with liposomes: requirement for cholesterol and virus receptors to allow fusion with and lysis of neutral but not of negatively charged liposomes. J Gen Virol 73 (Pt 11), 2831-2837 (1992).
9. Scolari, S. et al. Lateral distribution of the transmembrane domain of influenza virus hemagglutinin revealed by time-resolved fluorescence imaging. J Biol Chem 284, 15708-15716 (2009).
10. Scheiffele, P., Roth, M. G., Simons, K. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J 16, 5501-5508 (1997).
11. Leser, G. P., Lamb, R. A. Influenza virus assembly and budding in raft-derived microdomains: a quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology 342, 215-227 (2005).
12. Takeda, M., Leser, G. P., Russell, C. J., Lamb, R. A. Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion. Proc Natl Acad Sci USA 100, 14610-14617 (2003).
13. Hess, S. T. et al. Quantitative electron microscopy and fluorescence spectroscopy of the membrane distribution of influenza hemagglutinin. J Cell Biol 169, 965-976 (2005).
14. Scheiffele, P., Rietveld, A., Wilk, T., Simons, K. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J Biol Chem 274, 2038-2044 (1999).
15. Polozov, I. V., Bezrukov, L., Gawrisch, K., Zimmerberg, J. Progressive ordering with decreasing temperature of the phospholipids of influenza virus. Nat Chem Biol (2008).
16. Chlanda, P. et al. The hemifusion structure induced by Influenza virus haemagglutinin is determined by physical properties of the target membranes. Nat Microbiol 2016 (2016).
17. Meder, D., Moreno, M. J., Verkade, P., Vaz, W. L. C., Simons, K. Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 103, 329-334 (2006).
18. Veatch, S. L. et al. Critical fluctuations in plasma membrane vesicles. ACS Chem Biol 3, 287-293 (2008).
19. Veatch, S. L., Keller, S. L. Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys J 85, 3074-3083 (2003).
20. McConnell, H. M., Vrljic, M. Liquid-liquid immiscibility in membranes. Annu Rev Biophys Biomol Struct 32, 469-492 (2003).
21. Sezgin, E. et al. Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat Protoc 7, 1042-1051 (2012).
22. Beattie, M. E., Veatch, S. L., Stottrup, B. L., Keller, S. L. Sterol structure determines miscibility versus melting transitions in lipid vesicles. Biophysical Journal 89, 1760-1768 (2005).
23. Stottrup, B. L., Keller, S. L. Phase behavior of lipid monolayers containing DPPC and cholesterol analogs. Biophysical Journal 90, 3176-3183 (2006).
24. Barenholz, Y. Cholesterol and other membrane active sterols: from membrane evolution to "rafts". Prog Lipid Res 41, 1-5 (2002).
25. Miao, L. et al. From lanosterol to cholesterol: structural evolution and differential effects on lipid bilayers. Biophys J 82, 1429-1444 (2002).
26. Scheidt, H. A., Huster, D., Gawrisch, K. Diffusion of cholesterol and its precursors in lipid membranes studied by 1H pulsed field gradient magic angle spinning NMR. Biophys J 89, 2504-2512 (2005).
27. Xu, X., London, E. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 39, 843-849 (2000).
28. Petrache, H. I., Harries, D., Parsegian, V. A. Alteration of lipid membrane rigidity by cholesterol and its metabolic precursors. Macromolecular Symposia 219, 39-50 (2004).
29. Henriksen, J., Rowat, A. C., Ipsen, J. H. Vesicle fluctuation analysis of the effects of sterols on membrane bending rigidity. Eur Biophys J 33, 732-741 (2004).
30. Meleard, P. et al. Bending elasticities of model membranes: influences of temperature and sterol content. Biophys J 72, 2616-2629 (1997).
31. Bligh, E. G., Dyer, W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911-917 (1959).
32. Domanska, M. K. et al. Hemagglutinin Spatial Distribution Shifts in Response to Cholesterol in the Influenza Viral Envelope. Biophys J 109, 1917-1924 (2015).
33. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157, 38-46 (2007).
34. Bennett, W. F., MacCallum, J. L., Hinner, M. J., Marrink, S. J., Tieleman, D. P. Molecular view of cholesterol flip-flop and chemical potential in different membrane environments. J Am Chem Soc 131, 12714-12720 (2009).
35. Hamilton, J. A. Fast flip-flop of cholesterol and fatty acids in membranes: implications for membrane transport proteins. Curr Opin Lipidol 14, 263-271 (2003).
36. Kirby, C., Green, C. Transmembrane migration ('flip-flop') of cholesterol in erythrocyte membranes. Biochem J 168, 575-577 (1977).
37. Smith, R. J., Green, C. The rate of cholesterol 'flip-flop' in lipid bilayers and its relation to membrane sterol pools. FEBS Lett 42, 108-111 (1974).
38. Bacia, K., Schwille, P., Kurzchalia, T. Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc Natl Acad Sci USA 102, 3272-3277 (2005).
39. Cheetham, J. J., Epand, R. M., Andrews, M., Flanagan, T. D. Cholesterol sulfate inhibits the fusion of Sendai virus to biological and model membranes. J Biol Chem 265, 12404-12409 (1990).
40. Razinkov, V. I., Melikyan, G. B., Epand, R. M., Epand, R. F., Cohen, F. S. Effects of spontaneous bilayer curvature on influenza virus-mediated fusion pores. J Gen Physiol 112, 409-422 (1998).
41. Calder, L. J., Wasilewski, S., Berriman, J. A., Rosenthal, P. B. Structural organization of a filamentous influenza A virus. Proc Natl Acad Sci USA 107, 10685-10690 (2010).
42. Harris, A. et al. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci USA 103, 19123-19127 (2006).