Skip to main content
SpringerLink
Log in

Asymmetric Model Membranes: Frontiers and Challenges

  • Chapter
  • First Online:
Biomimetic Lipid Membranes: Fundamentals, Applications, and Commercialization

  • 821 Accesses

Abstract

Cellular membranes are highly complex liquid-crystalline entities, which makes it difficult for researchers to connect specific components and their effects on overall membrane structure, function, and biochemical and biophysical properties. To circumvent this issue, model membranes with controlled compositions have since become a staple of biomembrane research, helping researchers better understand the inner mechanisms of cell membranes. These simplified lipid systems have predominately been composed of symmetric lipid bilayers – where both leaflets are composed of the same constituents. Only recently has there been a shift toward the use of bilayer systems with asymmetric distributions of lipids across the two monolayers. This is because most (if not all) biological membranes possess lipid asymmetry which has sparked an intense desire to study its effects on membrane structure, dynamics, and membrane-associated molecules. In recent years, many have sought out to develop asymmetric model construction methods to facilitate these studies. In this chapter, we aim to describe novel and relevant asymmetric preparation methods, as well as their pros and cons to paint an image of the current state of biomembrane research and the challenges the field faces. Ultimately, these techniques are at the forefront of an exciting biomembrane renaissance.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. R.J. Alsop, L. Toppozini, D. Marquardt, N. Kuerka, T.A. Harroun, M.C. Rheinstadter, Aspirin inhibits formation of cholesterol rafts in fluid lipid membranes. Biochimica et Biophysica Acta (BBA) – Biomembranes 1848(3), 805–812 (2015)

    Google Scholar 

  2. H.D. Andersen, C. Wang, L. Arleth, G.H. Peters, P. Westh, Reconciliation of opposing views on membrane sugar interactions. Proc. Natl. Acad. Sci. 108(5), 1874–1878 (2011)

    Article  CAS  Google Scholar 

  3. T.G. Anderson, A. Tan, P. Ganz, J. Seelig, Calorimetric measurement of phospholipid interaction with methyl–cyclodextrin. Biochemistry 43(8), 2251–2261 (2004)

    Article  CAS  Google Scholar 

  4. A.G. Ayuyan, F.S. Cohen, Raft composition at physiological temperature and pH in the absence of detergents. Biophys. J. 94(7), 2654–2666 (2008)

    Article  CAS  Google Scholar 

  5. N.E. Barlow, E. Smpokou, M.S. Friddin, R. Macey, I.R. Gould, C. Turnbull, A.J. Flemming, N.J. Brooks, O. Ces, and L.M.C. Barter, Engineering plant membranes using droplet interface bilayers. Biomicrofluidics 11(2), 024107 (2017)

    Google Scholar 

  6. R.L. Biltonen, D. Lichtenberg, The use of differential scanning calorimetry as a tool to characterize liposome preparations. Chem. Phys. Lipids 64(1–3), 129–142 (1993)

    Article  CAS  Google Scholar 

  7. M.S. Bretscher, Asymmetrical lipid bilayer structure for biological membranes. Nat. New Biol. 236, 11–12 (1972)

    Article  CAS  Google Scholar 

  8. M.S. Bretscher, Membrane structure: some general principles. Science, New Series 181(4100), 622–629 (1973)

    CAS  Google Scholar 

  9. I. Burgess, M. Li, S. Horswell, G. Szymanski, J. Lipkowski, J. Majewski, S. Satija, Electric field-driven transformations of a supported model biological membrane an electrochemical and neutron reflectivity study. Biophys. J. 86(3), 1763–1776 (2004)

    Article  CAS  Google Scholar 

  10. A. Callan-Jones, B. Sorre, P. Bassereau, Curvature-driven lipid sorting in biomembranes. Cold Spring Harb. Perspect. Biol. 3(2), a004648–a004648 (2011)

    Article  CAS  Google Scholar 

  11. Y.H.M. Chan, S.G. Boxer, Model membrane systems and their applications. Curr. Opin. Chem. Biol. 11(6), 581–587 (2007)

    Article  CAS  Google Scholar 

  12. X. Chen, S. Liu, B. Deme, V. Cristiglio, D. Marquardt, R. Weller, P. Rao, Y. Wang, J. Bradshaw, Efficient internalization of TAT peptide in zwitterionic DOPC phospholipid membrane revealed by neutron diffraction. Biochim. Biophys. Acta Biomembr. 1859(5), 910–916 (2017)

    Article  CAS  Google Scholar 

  13. H.T. Cheng, E. London, Preparation and properties of asymmetric vesicles that mimic cell membranes: effect upon lipid raft formation and transmembrane helix orientation. J. Biol. Chem. 284(10), 6079–6092 (2009)

    Article  CAS  Google Scholar 

  14. H.T. Cheng, E. London, Preparation and properties of asymmetric large unilamellar vesicles: interleaflet coupling in asymmetric vesicles is dependent on temperature but not curvature. Biophys. J. 100(11), 2671–2678 (2011)

    Article  CAS  Google Scholar 

  15. S. Chiantia, E. London, Acyl chain length and saturation modulate interleaflet coupling in asymmetric bilayers: effects on dynamics and structural order. Biophys. J. 103(11), 2311–2319 (2012)

    Article  CAS  Google Scholar 

  16. S. Chiantia, P. Schwille, A.S. Klymchenko, E. London, Asymmetric GUVs prepared by MCD-mediated lipid exchange: an FCS study. Biophys. J. 100(1), L1–L3 (2011)

    Article  CAS  Google Scholar 

  17. E. Del Valle, Cyclodextrins and their uses: a review. Process Biochem. 39(9), 1033–1046 (2004)

    Article  CAS  Google Scholar 

  18. P.F. Devaux, Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30(5), 1163–1173 (1991)

    Article  CAS  Google Scholar 

  19. Y.M. Denkins, A.J. Schroit, Phosphatidylserine decarboxylase: generation of asymmetric vesicles and determination of the transbilayer distribution of fluorescent phosphatidylserine in model membrane systems. BBA – Biomembranes 862(2), 343–351 (1986)

    Article  CAS  Google Scholar 

  20. C. Dietrich, L. Bagatolli, Z. Volovyk, N. Thompson, M. Levi, K. Jacobson, E. Gratton, Lipid rafts reconstituted in model membranes. Biophys. J. 80(3), 1417–1428 (2001)

    Article  CAS  Google Scholar 

  21. M. Doktorova, F.A. Heberle, B. Eicher, F. Standaert, J. Katsaras, E. London, G. Pabst, D. Marquardt, Preparation of asymmetric phospholipid vesicles for use as cell membrane models. Nat. Protocols (2018). https://doi.org/10.1038/s41596-018-0033-6

  22. S.J. Eastman, M.J. Hope, P.R. Cullis, Transbilayer transport of phosphatidic acid in response to transmembrane pH gradients. Biochemistry 30(7), 1740–1745 (1991)

    Article  CAS  Google Scholar 

  23. M. Eeman, M. Deleu, From biological membranes to biomimetic model membranes. Biotechnol. Agron Soc. Environ. 14(4), 719–736 (2010)

    Google Scholar 

  24. B. Eicher, F.A. Heberle, D. Marquardt, G.N. Rechberger, J. Katsaras, G. Pabst, Joint small-angle X-ray and neutron scattering data analysis of asymmetric lipid vesicles. J. Appl. Crystallogr. 50(2), 419–429 (2017)

    Article  CAS  Google Scholar 

  25. B. Eicher, D. Marquardt, F.A. Heberle, I. Letofsky-Papst, G.N. Rechberger, M.S. Appavou, J. Katsaras, G. Pabst, Intrinsic curvature-mediated transbilayer coupling in asymmetric lipid vesicles. Biophys. J. 114(1), 146–157 (2018)

    Article  CAS  Google Scholar 

  26. Y. Elani, S. Purushothaman, P.J. Booth, J.M. Seddon, N.J. Brooks, R.V. Law, O. Ces, Measurements of the effect of membrane asymmetry on the mechanical properties of lipid bilayers. Chem. Commun. 6976(51), 6976–6979 (2015)

    Article  CAS  Google Scholar 

  27. P.V. Escriba, A. Ozaita, C. Ribas, A. Miralles, E. Fodor, T. Farkas, J.A. Garcia-Sevilla, Role of lipid polymorphism in G protein-membrane interactions: nonlamellar-prone phospholipids and peripheral protein binding to membranes. Proc. Natl. Acad. Sci. 94(21), 11375–11380 (1997)

    Article  CAS  Google Scholar 

  28. S. Fujii, T. Matsuura, T. Sunami, Y. Kazuta, T. Yomo, In vitro evolution of -hemolysin using a liposome display. Proc. Natl. Acad. Sci. 110(42), 16796–16801 (2013)

    Article  CAS  Google Scholar 

  29. V. Gerke, C.E. Creutz, S.E. Moss, Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6(6), 449–461 (2005)

    Article  CAS  Google Scholar 

  30. M. Gotanda, K. Kamiya, T. Osaki, S. Fujii, N. Misawa, N. Miki, S. Takeuchi, Sequential generation of asymmetric lipid vesicles using a pulsed-jetting method in rotational wells. Sensors Actuators B Chem. 261, 392–397 (2018)

    Article  CAS  Google Scholar 

  31. T. Hamada, Y. Miura, Y. Komatsu, Y. Kishimoto, M. Vestergaard, M. Takagi, Construction of asymmetric cell-sized lipid vesicles from lipid-coated water-in-oil microdroplets. J. Phys. Chem. B 112(47), 14678–14681 (2008)

    Article  CAS  Google Scholar 

  32. F.A. Heberle, D. Marquardt, M. Doktorova, B. Geier, R.F. Standaert, P. Heftberger, B. Kollmitzer, J.D. Nickels, R.A. Dick, G.W. Feigenson, J. Katsaras, E. London, G. Pabst, Sub-nanometer structure of an asymmetric model membrane: interleaflet coupling influences domain properties. Langmuir 32(20), 5195–5200 (2016)

    Article  CAS  Google Scholar 

  33. E.K. Hoffmann, L.O. Simonsen, Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol. Rev. 69(2), 315–382 (1989)

    Article  CAS  Google Scholar 

  34. J.M. Holopainen, M.I. Angelova, P.K. Kinnunen, Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys. J. 78(2), 830–838 (2000)

    Article  CAS  Google Scholar 

  35. M. Holzer, J. Momm, R. Schubert, Lipid transfer mediated by a recombinant pro-sterol carrier protein 2 for the accurate preparation of asymmetrical membrane vesicles requires a narrow vesicle size distribution: a free-flow electrophoresis study. Langmuir 26(6), 4142–4151 (2010)

    Article  CAS  Google Scholar 

  36. M.J. Hope, P.R. Cullis, Lipid asymmetry induced by transmembrane pH gradients in large unilamellar vesicles. J. Biol. Chem. 262(9), 4360–4366 (1987)

    CAS  Google Scholar 

  37. M.J. Hope, T.E. Redelmeier, K.F. Wong, W. Rodrigueza, P.R. Cullis, Phospholipid asymmetry in large unilamellar vesicles induced by transmembrane pH gradients. Biochemistry 28(10), 4181–4187 (1989)

    Article  CAS  Google Scholar 

  38. P.C. Hu, S. Li, N. Malmstadt, Microfluidic fabrication of asymmetric giant lipid vesicles. ACS Appl. Mater. Interfaces 3(5), 1434–1440 (2011)

    Article  CAS  Google Scholar 

  39. Z. Huang, E. London, Effect of cyclodextrin and membrane lipid structure upon cyclodextrin lipid interaction. Langmuir 29(47), 14631–14638 (2013)

    Article  CAS  Google Scholar 

  40. W.L. Hwang, M. Chen, B. Cronin, M.A. Holden, H. Bayley, Asymmetric droplet interface bilayers. J. Am. Chem. Soc. 130(18), 5878–5879 (2008)

    Article  CAS  Google Scholar 

  41. L.W. Johnson, M.E. Hughes, D.B. Zilversmit, Use of phospholipid exchange protein to measure inside-outside transposition in phosphatidylcholine liposomes. BBA – Biomembranes 375(2), 176–185 (1975)

    Article  CAS  Google Scholar 

  42. S.Y. Jung, S.T. Retterer, C.P. Collier, On-demand generation of monodisperse femtolitre droplets by shape-induced shear. Lab Chip 10(20), 2688–2694 (2010)

    Article  CAS  Google Scholar 

  43. K. Kamiya, T. Osaki, S. Fujii, N. Misawa, S. Takeuchi, Nano-sized asymmetric lipid vesicles for drug carrier applications, in Proceedings of the IEEE International Conference on Micro Electro Mechanical Systems (MEMS), vol. 2018, 2018, pp. 152–153

    Google Scholar 

  44. K. Karamdad, R.V. Law, J.M. Seddon, N.J. Brooks, O. Ces, Studying the effects of asymmetry on the bending rigidity of lipid membranes formed by microfluidics. Chem. Commun. 52(30), 5277–5280 (2016)

    Article  CAS  Google Scholar 

  45. R.D. Kornberg, H.M. McConnell, Lateral diffusion of phospholipids in a vesicle membrane. Proc. Natl. Acad. Sci. 68(10), 2564–2568 (1971)

    Article  CAS  Google Scholar 

  46. N. Kučerka, D. Marquardt, T.A. Harroun, M.P. Nieh, S.R. Wassall, de Jong DH, L.V. Schäfer, S.J. Marrink, J. Katsaras, Cholesterol in bilayers with PUFA chains: doping with DMPC or POPC results in sterol reorientation and membrane-domain formation. Biochemistry 49(35), 7485–7493 (2010)

    Google Scholar 

  47. B.R. Lentz, Exposure of platelet membrane phosphatidylserine regulates blood coagulation. Prog. Lipid Res. 42(5), 423–438 (2003)

    Article  CAS  Google Scholar 

  48. R. Leventis, J.R. Silvius, Use of cyclodextrins to monitor transbilayer movement and differential lipid affinities of cholesterol. Biophys. J. 81(4), 2257–2267 (2001)

    Article  CAS  Google Scholar 

  49. T. Lhermusier, H. Chap, B. Payrastre, Platelet membrane phospholipid asymmetry: from the characterization of a scramblase activity to the identification of an essential protein mutated in Scott syndrome: platelet phospholipid scramblase. J. Thromb. Haemost. 9(10), 1883–1891 (2011)

    Article  CAS  Google Scholar 

  50. G. Li, J. Kim, Z. Huang, J.R. St Clair, D.A. Brown, E. London, Efficient replacement of plasma membrane outer leaflet phospholipids and sphingolipids in cells with exogenous lipids. Proc. Natl. Acad. Sci. 113(49), 14025–14030 (2016)

    Article  CAS  Google Scholar 

  51. M.O. Li, Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 302(5650), 1560–1563 (2003)

    Article  CAS  Google Scholar 

  52. L. Lu, J.W. Schertzer, P.R. Chiarot, Continuous microfluidic fabrication of synthetic asymmetric vesicles. Lab Chip 15(17), 3591–3599 (2015)

    Article  CAS  Google Scholar 

  53. D. Marquardt, J.A. Williams, N. Kučerka, J. Atkinson, S.R. Wassall, J. Katsaras, T.A. Harroun, Tocopherol activity correlates with its location in a membrane: a new perspective on the antioxidant vitamin E. J. Am. Chem. Soc. 135(20), 7523–7533 (2013)

    Article  CAS  Google Scholar 

  54. D. Marquardt, B. Geier, G. Pabst, Asymmetric lipid membranes: towards more realistic model systems. Membranes 5(2), 180–196 (2015)

    Article  CAS  Google Scholar 

  55. D. Marquardt, F.A. Heberle, J.D. Nickels, G. Pabst, J. Katsaras, On scattered waves and lipid domains: detecting membrane rafts with X-rays and neutrons. Soft Matter 11(47), 9055–9072 (2015)

    Article  CAS  Google Scholar 

  56. D. Marquardt, F.A. Heberle, T. Miti, B. Eicher, E. London, J. Katsaras, G. Pabst, 1H NMR shows slow phospholipid flip-flop in gel and fluid bilayers. Langmuir 33(15), 3731–3741 (2017)

    Article  CAS  Google Scholar 

  57. S. Matosevic, B.M. Paegel, Layer-by-layer cell membrane assembly. Nat. Chem. 5(11), 958–963 (2013)

    Article  CAS  Google Scholar 

  58. G. van Meer, Dynamic transbilayer lipid asymmetry. Cold Spring Harb. Perspect. Biol. 3(5), 1–11 (2011)

    Google Scholar 

  59. A.A. Mokhtarieh, J. Lee, S. Kim, M.K. Lee, Preparation of siRNA encapsulated nanoliposomes suitable for siRNA delivery by simply discontinuous mixing. Biochim. Biophys. Acta Biomembr. 1860(6), 1318–1325 (2018)

    Article  CAS  Google Scholar 

  60. M. Mulder, Basic Principles of Membrane Technology, Klewer Academic Publishers: Dordrecht, vol. 72 (1996)

    Google Scholar 

  61. M. Nakano, M. Fukuda, T. Kudo, H. Endo, T. Handa, Determination of interbilayer and transbilayer lipid transfers by time-resolved small-angle neutron scattering. Phys. Rev. Lett. 98(23), 238101 (2007)

    Google Scholar 

  62. M. Nakano, M. Fukuda, T. Kudo, N. Matsuzaki, T. Azuma, K. Sekine, H. Endo, T. Handa, Flip-flop of phospholipids in vesicles: kinetic analysis with time-resolved small-angle neutron scattering. J. Phys. Chem. B 113(19), 6745–6748 (2009)

    Article  CAS  Google Scholar 

  63. M.A. Nguyen, G. Taylor, S. Sarles, A microfluidic assembly and simultaneous interrogation of networks of asymmetric biomimetic membranes, in ASME 2017 Conference on Smart Materials, Adaptive Structures and Intelligent Systems, SMASIS 2017, vol. 1, 2017

    Google Scholar 

  64. G.L. Nicolson, The fluid-mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochimica et Biophysica Acta (BBA) – Biomembranes 6, 1451–1466 (2014)

    Article  CAS  Google Scholar 

  65. N. Kučerka, M.-P. Nieh, J. Katsaras, Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochim. Biophys. Acta 1808, 2761–2771 (2011)

    Article  CAS  Google Scholar 

  66. M. Otsuka, T. Matsumoto, R. Morimoto, S. Arioka, H. Omote, Y. Moriyama, A human transporter protein that mediates the final excretion step for toxic organic cations. Proc. Natl. Acad. Sci. 102(50), 17923–17928 (2005)

    Article  CAS  Google Scholar 

  67. S. Pautot, B.J. Frisken, D.A. Weitz, Engineering asymmetric vesicles. Proc. Natl. Acad. Sci. 100(19), 10718–10721 (2003)

    Article  CAS  Google Scholar 

  68. Q. Lin, E. London, Preparation of artificial plasma membrane mimicking vesicles with lipid asymmetry. PLoS One 9(1), e87903 (2014)

    Google Scholar 

  69. J.E. Rothman, J. Lenard, Membrane asymmetry. Science, New Series 195(4280), 743–753 (1977)

    CAS  Google Scholar 

  70. S.S. Sheu, Transmembrane Na+ and Ca2+ electrochemical gradients in cardiac muscle and their relationship to force development. J. Gen. Physiol. 80(3), 325–351 (1982)

    Article  CAS  Google Scholar 

  71. K. Simons, W.L. Vaz, Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33(1), 269–295 (2004)

    Article  CAS  Google Scholar 

  72. C.E. Stanley, K.S. Elvira, X.Z. Niu, A.D. Gee, O. Ces, J.B. Edel, A.J. Demello, A microfluidic approach for high-throughput droplet interface bilayer (DIB) formation. Chem. Commun. 46(10), 1620–1622 (2010)

    Article  CAS  Google Scholar 

  73. C. Steenbergen, M.L. Hill, R.B. Jennings, Volume regulation and plasma membrane injury in aerobic, anaerobic, and ischemic myocardium in vitro. Effects of osmotic cell swelling on plasma membrane integrity. Circ. Res. 57(6), 864–875 (1985)

    CAS  Google Scholar 

  74. R. Takaoka, H. Kurosaki, H. Nakao, K. Ikeda, M. Nakano, Formation of asymmetric vesicles via phospholipase D-mediated transphosphatidylation. Biochim. Biophys. Acta Biomembr. 1860(2), 245–249 (2018)

    Article  CAS  Google Scholar 

  75. K. Tanaka, K. Fujimura-Kamada, T. Yamamoto, Functions of phospholipid flippases. J. Biochem. 149(2), 131–143 (2011)

    Article  CAS  Google Scholar 

  76. G.J. Taylor, S.A. Sarles, Model neural membrane droplet interface bilayers from brain total lipid extract for studying membrane-peptide interactions with amyloid, in MRS Proceedings, vol. 1722, 2015

    Google Scholar 

  77. K. Tsumoto, H. Matsuo, M. Tomita, T. Yoshimura, Efficient formation of giant liposomes through the gentle hydration of phosphatidylcholine films doped with sugar. Colloids Surf. B Biointerfaces 68(1), 98–105 (2009)

    Article  CAS  Google Scholar 

  78. K. Uekama, F. Hirayama, T. Irie, Cyclodextrin drug carrier systems. Chem. Rev. 98(5), 2045–2076 (1998)

    Article  CAS  Google Scholar 

  79. D. Van Swaay, A. Demello, Microfluidic methods for forming liposomes (2013). https://doi.org/10.1039/c2lc41121k

  80. M.P. Veiga, Arrondo JLR, Goñi FM, A. Alonso, Ceramides in phospholipid membranes: effects on bilayer stability and transition to nonlamellar phases. Biophys. J. 76(1), 342–350 (1999)

    Google Scholar 

  81. A.J. Verkleij, R.F.A. Zwaal, B. Roelofsen, P. Comfurius, D. Kastelijn, L.L.M. van Deenen, The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim. Biophys. Acta Biomembr. 323(2), 178–193 (1973)

    Article  CAS  Google Scholar 

  82. J. Vicogne, D. Vollenweider, J.R. Smith, P. Huang, M.A. Frohman, J.E. Pessin, Asymmetric phospholipid distribution drives in vitro reconstituted SNARE-dependent membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 103(40), 14761–14766 (2006)

    Article  CAS  Google Scholar 

  83. M.L. Wagner, L.K. Tamm, Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: silane-polyethyleneglycol-lipid as a cushion and covalent linker. Biophys. J. 79(3), 1400–1414 (2000)

    Article  CAS  Google Scholar 

  84. J. Weinberg, D.G. Drubin, Clathrin-mediated endocytosis in budding yeast. Trends Cell Biol. 22(1), 1–13 (2012)

    Article  CAS  Google Scholar 

  85. G.M. Whitesides, The origins and the future of microfluidics. Nature 442(7101), 368–373 (2006)

    Article  CAS  Google Scholar 

  86. K.W. Wirtz, D.B. Zilversmit, Exchange of phospholipids between liver mitochondria and microsomes in vitro. J. Biol. Chem. 243(13), 3596–3602 (1968)

    CAS  Google Scholar 

  87. A. Zachowski, Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294, 1–14 (1993)

    Article  CAS  Google Scholar 

  88. Q. Zhou, J. Zhao, J.G. Stout, R.A. Luhm, T. Wiedmer, P.J. Sims, Molecular cloning of human plasma membrane phospholipid scramblase: a protein mediating transbilayer movement of plasma membrane phospholipids. J. Biol. Chem. 272(29), 18240–18244 (1997)

    Article  CAS  Google Scholar 

  89. D.B. Zilversmit, Lipid transfer proteins: overview and applications. Methods Enzymol. 98(C), 565–573 (1983)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work acknowledges support from the Natural Sciences and Engineering Research Council (NSERC) of Canada.

Author information

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, University of Windsor, Windsor, ON, Canada

    Michael H. L. Nguyen, Brett W. Rickeard, Mitchell DiPasquale & Drew Marquardt

Authors
  1. Michael H. L. Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brett W. Rickeard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mitchell DiPasquale
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Drew Marquardt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Drew Marquardt .

Editor information

Editors and Affiliations

  1. Department of Molecular Biology and Genetics, İstanbul Technical University, Istanbul, Turkey

    Fatma N. Kök

  2. Department of Bioengineering, Izmir Institute of Technology, Urla, Izmir, Turkey

    Ahu Arslan Yildiz

  3. School of Medicine, Stanford University, Palo Alto, CA, USA

    Fatih Inci

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Nguyen, M.H.L., Rickeard, B.W., DiPasquale, M., Marquardt, D. (2019). Asymmetric Model Membranes: Frontiers and Challenges. In: Kök, F., Arslan Yildiz, A., Inci, F. (eds) Biomimetic Lipid Membranes: Fundamentals, Applications, and Commercialization. Springer, Cham. https://doi.org/10.1007/978-3-030-11596-8_3

Download citation

Publish with us

Policies and ethics

Search

Navigation