Skip to main content

Nanodiscs as a New Tool to Examine Lipid–Protein Interactions

  • Protocol
  • First Online:
Lipid-Protein Interactions

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2003))

Abstract

The interactions between lipids and proteins are one of the most fundamental processes in living organisms, responsible for critical cellular events ranging from replication, cell division, signaling, and movement. Enabling the central coupling responsible for maintaining the functionality of the breadth of proteins, receptors, and enzymes that find their natural home in biological membranes, the fundamental mechanisms of recognition of protein for lipid, and vice versa, have been a focal point of biochemical and biophysical investigations for many decades. Complexes of lipids and proteins, such as the various lipoprotein factions, play central roles in the trafficking of important proteins, small molecules and metabolites and are often implicated in disease states. Recently an engineered lipoprotein particle, termed the nanodisc, a modified form of the human high density lipoprotein fraction, has served as a membrane mimetic for the investigation of membrane proteins and studies of lipid–protein interactions. In this review, we summarize the current knowledge regarding this self-assembling lipid–protein complex and provide examples for its utility in the investigation of a large number of biological systems.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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. Carlson JW, Jonas A, Sligar SG (1997) Imaging and manipulation of high-density lipoproteins. Biophys J 73(3):1184–1189. https://doi.org/10.1016/s0006-3495(97)78150-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bayburt TH, Carlson JW, Sligar SG (1998) Reconstitution and imaging of a membrane protein in a nanometer-size phospholipid bilayer. J Struct Biol 123(1):37–44. https://doi.org/10.1006/jsbi.1998.4007

    Article  CAS  PubMed  Google Scholar 

  3. Jonas A (1986) Reconstitution of high-density lipoproteins. Methods Enzymol 128:553–582

    Article  CAS  Google Scholar 

  4. Matz CE, Jonas A (1982) Micellar complexes of human apolipoprotein A-I with phosphatidylcholines and cholesterol prepared from cholate-lipid dispersions. J Biol Chem 257(8):4535–4540

    CAS  PubMed  Google Scholar 

  5. Beck von Bodman S, Schuler MA, Jollie DR, Sligar SG (1986) Synthesis, bacterial expression, and mutagenesis of the gene coding for mammalian cytochrome b5. Proc Natl Acad Sci U S A 83(24):9443–9447

    Article  CAS  Google Scholar 

  6. Bayburt TH, Grinkova YV, Sligar SG (2002) Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett 2(8):853–856. https://doi.org/10.1021/nl025623k

    Article  CAS  Google Scholar 

  7. Denisov IG, Grinkova YV, Lazarides AA, Sligar SG (2004) Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J Am Chem Soc 126(11):3477–3487

    Article  CAS  Google Scholar 

  8. Grinkova YV, Denisov IG, Sligar SG (2010) Engineering extended membrane scaffold proteins for self-assembly of soluble nanoscale lipid bilayers. Protein Eng Des Sel 23(11):843–848. https://doi.org/10.1093/protein/gzq060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bayburt TH, Carlson JW, Sligar SG (2000) Single molecule height measurements on a membrane protein in nanometer-scale phospholipid bilayer disks. Langmuir 16(14):5993–5997. https://doi.org/10.1021/la991449c

    Article  CAS  Google Scholar 

  10. Bayburt TH, Sligar SG (2002) Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks. Proc Natl Acad Sci U S A 99(10):6725–6730. https://doi.org/10.1073/pnas.062565599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bayburt TH, Sligar SG (2003) Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers. Protein Sci 12(11):2476–2481. https://doi.org/10.1110/ps.03267503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Civjan NR, Bayburt TH, Schuler MA, Sligar SG (2003) Direct solubilization of heterologously expressed membrane proteins by incorporation into nanoscale lipid bilayers. BioTechniques 35(3):556–558, 560, 562–563

    Article  CAS  Google Scholar 

  13. Denisov IG, Sligar SG (2016) Nanodiscs for structural and functional studies of membrane proteins. Nat Struct Mol Biol 23(6):481–486. https://doi.org/10.1038/nsmb.3195

    Article  CAS  PubMed  Google Scholar 

  14. Denisov IG, Sligar SG (2017) Nanodiscs in membrane biochemistry and biophysics. Chem Rev 117(6):4669–4713. https://doi.org/10.1021/acs.chemrev.6b00690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Li Y, Kijac AZ, Sligar SG, Rienstra CM (2006) Structural analysis of nanoscale self-assembled discoidal lipid bilayers by solid-state NMR spectroscopy. Biophys J 91(10):3819–3828. https://doi.org/10.1529/biophysj.106.087072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Phillips JC, Wriggers W, Li Z, Jonas A, Schulten K (1997) Predicting the structure of apolipoprotein A-I in reconstituted high-density lipoprotein disks. Biophys J 73(5):2337–2346. https://doi.org/10.1016/s0006-3495(97)78264-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wlodawer A, Segrest JP, Chung BH, Chiovetti R Jr, Weinstein JN (1979) High-density lipoprotein recombinants: evidence for a bicycle tire micelle structure obtained by neutron scattering and electron microscopy. FEBS Lett 104(2):231–235

    Article  CAS  Google Scholar 

  18. Shih AY, Denisov IG, Phillips JC, Sligar SG, Schulten K (2005) Molecular dynamics simulations of discoidal bilayers assembled from truncated human lipoproteins. Biophys J 88(1):548–556. https://doi.org/10.1529/biophysj.104.046896

    Article  CAS  PubMed  Google Scholar 

  19. Hagn F, Etzkorn M, Raschle T, Wagner G (2013) Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J Am Chem Soc 135(5):1919–1925. https://doi.org/10.1021/ja310901f

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Siuda I, Tieleman DP (2015) Molecular models of nanodiscs. J Chem Theory Comput 11(10):4923–4932. https://doi.org/10.1021/acs.jctc.5b00668

    Article  CAS  PubMed  Google Scholar 

  21. Mendelsohn R, Davies MA, Brauner JW, Schuster HF, Dluhy RA (1989) Quantitative determination of conformational disorder in the acyl chains of phospholipid bilayers by infrared spectroscopy. Biochemistry 28(22):8934–8939

    Article  CAS  Google Scholar 

  22. Lins L, Brasseur R, Rosseneu M, Vanloo B, Ruysschaert JM (1993) Structure of the apolipoprotein A-IV/lipid discoidal complexes: an attenuated total reflection polarized Fourier transform infrared spectroscopy study. Biochim Biophys Acta 1149(2):267–277

    Article  CAS  Google Scholar 

  23. Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta 1469(3):159–195

    Article  CAS  Google Scholar 

  24. Tristram-Nagle S, Nagle JF (2004) Lipid bilayers: thermodynamics, structure, fluctuations, and interactions. Chem Phys Lipids 127(1):3–14

    Article  CAS  Google Scholar 

  25. Vestergaard M, Kraft JF, Vosegaard T, Thogersen L, Schiott B (2015) Bicelles and other membrane mimics: comparison of structure, properties, and dynamics from MD simulations. J Phys Chem B 119(52):15831–15843. https://doi.org/10.1021/acs.jpcb.5b08463

    Article  CAS  PubMed  Google Scholar 

  26. Debnath A, Schafer LV (2015) Structure and dynamics of phospholipid Nanodiscs from all-atom and coarse-grained simulations. J Phys Chem B 119(23):6991–7002. https://doi.org/10.1021/acs.jpcb.5b02101

    Article  CAS  PubMed  Google Scholar 

  27. Hsu PC, Bruininks BMH, Jefferies D, Cesar Telles de Souza P, Lee J, Patel DS, Marrink SJ, Qi Y, Khalid S, Im W (2017) CHARMM-GUI Martini Maker for modeling and simulation of complex bacterial membranes with lipopolysaccharides. J Comput Chem 38(27):2354–2363. https://doi.org/10.1002/jcc.24895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Denisov IG, McLean MA, Shaw AW, Grinkova YV, Sligar SG (2005) Thermotropic phase transition in soluble nanoscale lipid bilayers. J Phys Chem B 109(32):15580–15588. https://doi.org/10.1021/jp051385g

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Shaw AW, McLean MA, Sligar SG (2004) Phospholipid phase transitions in homogeneous nanometer scale bilayer discs. FEBS Lett 556(1–3):260–264

    Article  CAS  Google Scholar 

  30. Gennis RB (1989) Biomembranes. Molecular structure and function. Springer, New York

    Book  Google Scholar 

  31. Marsh D (2008) Protein modulation of lipids, and vice-versa, in membranes. Biochim Biophys Acta 1778(7–8):1545–1575. https://doi.org/10.1016/j.bbamem.2008.01.015

    Article  CAS  PubMed  Google Scholar 

  32. Marsh D (2010) Electron spin resonance in membrane research: protein-lipid interactions from challenging beginnings to state of the art. Eur Biophys J 39(4):513–525. https://doi.org/10.1007/s00249-009-0512-3

    Article  CAS  PubMed  Google Scholar 

  33. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11(10):688–699. https://doi.org/10.1038/nrm2977

    Article  CAS  PubMed  Google Scholar 

  34. He HT, Marguet D (2011) Detecting nanodomains in living cell membrane by fluorescence correlation spectroscopy. Annu Rev Phys Chem 62:417–436. https://doi.org/10.1146/annurev-physchem-032210-103402

    Article  CAS  PubMed  Google Scholar 

  35. Needham D, Evans E (1988) Structure and mechanical properties of giant lipid (DMPC) vesicle bilayers from 20 degrees C below to 10 degrees C above the liquid crystal-crystalline phase transition at 24 degrees C. Biochemistry 27(21):8261–8269

    Article  CAS  Google Scholar 

  36. Cevc G (ed) (1993) Phospholipids handbook. Marcel Dekker, Inc, New York

    Google Scholar 

  37. Bayburt TH, Sligar SG (2010) Membrane protein assembly into nanodisks. FEBS Lett 584(9):1721–1727. https://doi.org/10.1016/j.febslet.2009.10.024

    Article  CAS  PubMed  Google Scholar 

  38. Leitz AJ, Bayburt TH, Barnakov AN, Springer BA, Sligar SG (2006) Functional reconstitution of β2-adrenergic receptors utilizing self-assembling nanodisc technology. BioTechniques 40(5):601–602, 604, 606, 608, 610, 612. https://doi.org/10.2144/000112169

    Article  CAS  PubMed  Google Scholar 

  39. Whorton MR, Bokoch MP, Rasmussen SGF, Huang B, Zare RN, Kobilka B, Sunhara RK (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc Natl Acad Sci U S A 104(18):7682–7687

    Article  CAS  Google Scholar 

  40. Whorton MR, Jastrzebska B, Park PSH, Fotiadis D, Engel A, Palczewski K, Sunahara RK (2008) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J Biol Chem 283(7):4387–4394

    Article  CAS  Google Scholar 

  41. Bayburt TH, Vishnivetskiy SA, McLean MA, Morizumi T, Huang C-C, Tesmer JJG, Ernst OP, Sligar SG, Gurevich VV (2011) Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and Arrestin-1 binding. J Biol Chem 286(2):1420–1428. https://doi.org/10.1074/jbc.M110.151043

    Article  CAS  PubMed  Google Scholar 

  42. Knepp AM, Grunbeck A, Banerjee S, Sakmar TP, Huber T (2011) Direct measurement of thermal stability of expressed CCR5 and stabilization by small molecule ligands. Biochemistry 50(4):502–511. https://doi.org/10.1021/bi101059w

    Article  CAS  PubMed  Google Scholar 

  43. Goldsmith BR, Mitala JJ Jr, Josue J, Castro A, Lerner MB, Bayburt TH, Khamis SM, Jones RA, Brand JG, Sligar SG, Luetje CW, Gelperin A, Rhodes PA, Discher BM, Johnson ATC (2011) Biomimetic chemical sensors using nanoelectronic readout of olfactory receptor proteins. ACS Nano 5(7):5408–5416. https://doi.org/10.1021/nn200489j

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Orban E, Proverbio D, Haberstock S, Doetsch V, Bernhard F (2015) Cell-free expression of G-protein-coupled receptors. Methods Mol Biol 1261:171–195. https://doi.org/10.1007/978-1-4939-2230-7_10

    Article  CAS  PubMed  Google Scholar 

  45. Casiraghi M, Damian M, Lescop E, Point E, Moncoq K, Morellet N, Levy D, Marie J, Guittet E, Baneres JL, Catoire LJ (2016) Functional modulation of a G protein-coupled receptor conformational landscape in a lipid bilayer. J Am Chem Soc 138(35):11170–11175. https://doi.org/10.1021/jacs.6b04432

    Article  CAS  PubMed  Google Scholar 

  46. Hansen RW, Wang X, Golab A, Bornert O, Oswald C, Wagner R, Martinez KL (2016) Functional stability of the human kappa opioid receptor reconstituted in nanodiscs revealed by a time-resolved scintillation proximity assay. PLoS One 11(4):e0150658/0150651–e0150658/0150618. https://doi.org/10.1371/journal.pone.0150658

    Article  CAS  Google Scholar 

  47. Scarselli M, Annibale P, McCormick PJ, Kolachalam S, Aringhieri S, Radenovic A, Corsini GU, Maggio R (2016) Revealing G-protein-coupled receptor oligomerization at the single-molecule level through a nanoscopic lens: methods, dynamics and biological function. FEBS J 283(7):1197–1217. https://doi.org/10.1111/febs.13577

    Article  CAS  PubMed  Google Scholar 

  48. Raschle T, Hiller S, Yu T-Y, Rice AJ, Walz T, Wagner G (2009) Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs. J Am Chem Soc 131(49):17777–17779

    Article  CAS  Google Scholar 

  49. Yu T-Y, Raschle T, Hiller S, Wagner G (2012) Solution NMR spectroscopic characterization of human VDAC-2 in detergent micelles and lipid bilayer nanodiscs. Biochim Biophys Acta 1818(6):1562–1569. https://doi.org/10.1016/j.bbamem.2011.11.012

    Article  CAS  PubMed  Google Scholar 

  50. Shenkarev ZO, Lyukmanova EN, Paramonov AS, Shingarova LN, Chupin VV, Kirpichnikov MP, Blommers MJJ, Arseniev AS (2010) Lipid-protein nanodiscs as reference medium in detergent screening for high-resolution NMR studies of integral membrane proteins. J Am Chem Soc 132(16):5628–5629

    Article  CAS  Google Scholar 

  51. Shenkarev ZO, Paramonov AS, Lyukmanova EN, Shingarova LN, Yakimov SA, Dubinnyi MA, Chupin VV, Kirpichnikov MP, Blommers MJJ, Arseniev AS (2010) NMR structural and dynamical investigation of the isolated voltage-sensing domain of the potassium channel KvAP: implications for voltage gating. J Am Chem Soc 132(16):5630–5637

    Article  CAS  Google Scholar 

  52. Autzen HE, Myasnikov AG, Campbell MG, Asarnow D, Julius D, Cheng Y (2018) Structure of the human TRPM4 ion channel in a lipid nanodisc. Science 359(6372):228–232. https://doi.org/10.1126/science.aar4510

    Article  CAS  PubMed  Google Scholar 

  53. Stam NJ, Wilkens S (2017) Structure of the lipid nanodisc-reconstituted vacuolar ATPase proton channel: definition of the interaction of rotor and stator and implications for enzyme regulation by reversible dissociation. J Biol Chem 292(5):1749–1761. https://doi.org/10.1074/jbc.M116.766790

    Article  CAS  PubMed  Google Scholar 

  54. Paramonov AS, Lyukmanova EN, Myshkin MY, Shulepko MA, Kulbatskii DS, Petrosian NS, Chugunov AO, Dolgikh DA, Kirpichnikov MP, Arseniev AS, Shenkarev ZO (2017) NMR investigation of the isolated second voltage-sensing domain of human Nav1.4 channel. Biochim Biophys Acta Biomembr 1859(3):493–506. https://doi.org/10.1016/j.bbamem.2017.01.004

    Article  CAS  PubMed  Google Scholar 

  55. Dang S, Feng S, Tien J, Peters CJ, Bulkley D, Lolicato M, Zhao J, Zuberbuhler K, Ye W, Qi L, Chen T, Craik CS, Nung Jan Y, Minor DL Jr, Cheng Y, Yeh Jan L (2017) Cryo-EM structures of the TMEM16A calcium-activated chloride channel. Nature 552(7685):426–429. https://doi.org/10.1038/nature25024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Chen Q, She J, Zeng W, Guo J, Xu H, Bai XC, Jiang Y (2017) Structure of mammalian endolysosomal TRPML1 channel in nanodiscs. Nature 550(7676):415–418. https://doi.org/10.1038/nature24035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Shen PS, Yang X, DeCaen PG, Liu X, Bulkley D, Clapham DE, Cao E (2016) The structure of the polycystic kidney disease channel PKD2 in lipid nanodiscs. Cell 167(3):763–773.e711. https://doi.org/10.1016/j.cell.2016.09.048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sadler EE, Kapanidis AN, Tucker SJ (2016) Solution-based single-molecule FRET studies of K(+) channel gating in a lipid bilayer. Biophys J 110(12):2663–2670. https://doi.org/10.1016/j.bpj.2016.05.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Matthies D, Dalmas O, Borgnia Mario J, Dominik Pawel K, Merk A, Rao P, Reddy Bharat G, Islam S, Bartesaghi A, Perozo E, Subramaniam S (2016) Cryo-EM structures of the magnesium channel CorA reveal symmetry break upon gating. Cell 164(4):747–756. https://doi.org/10.1016/j.cell.2015.12.055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Gao Y, Cao E, Julius D, Cheng Y (2016) TRPV1 structures in nanodiscs reveal mechanisms of ligand and lipid action. Nature 534(7607):347–351. https://doi.org/10.1038/nature17964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Alami M, Dalal K, Lelj-Garolla B, Sligar SG, Duong F (2007) Nanodiscs unravel the interaction between the SecYEG channel and its cytosolic partner SecA. EMBO J 26(8):1995–2004. https://doi.org/10.1038/sj.emboj.7601661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Dalal K, Duong F (2010) Reconstitution of the SecY translocon in nanodiscs. Methods Mol Biol 619:145–156. https://doi.org/10.1007/978-1-60327-412-8_9

    Article  CAS  PubMed  Google Scholar 

  63. Dalal K, Nguyen N, Alami M, Tan J, Moraes TF, Lee WC, Maurus R, Sligar SS, Brayer GD, Duong F (2009) Structure, binding, and activity of Syd, a SecY-interacting protein. J Biol Chem 284(12):7897–7902

    Article  CAS  Google Scholar 

  64. Kawai T, Caaveiro JM, Abe R, Katagiri T, Tsumoto K (2011) Catalytic activity of MsbA reconstituted in nanodisc particles is modulated by remote interactions with the bilayer. FEBS Lett 585(22):3533–3537. https://doi.org/10.1016/j.febslet.2011.10.015

    Article  CAS  PubMed  Google Scholar 

  65. Ritchie TK, Kwon H, Atkins WM (2011) Conformational analysis of human ATP-binding cassette transporter ABCB1 in lipid nanodiscs and inhibition by the antibodies MRK16 and UIC2. J Biol Chem 286(45):39489–39496. https://doi.org/10.1074/jbc.M111.284554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Zwaal RF, Comfurius P, Bevers EM (1998) Lipid-protein interactions in blood coagulation. Biochim Biophys Acta 1376(3):433–453

    Article  CAS  Google Scholar 

  67. Daury L, Orange F, Taveau J-C, Verchere A, Monlezun L, Gounou C, Marreddy RKR, Picard M, Broutin I, Pos KM, Lambert O (2016) Tripartite assembly of RND multidrug efflux pumps. Nat Commun 7:10731. https://doi.org/10.1038/ncomms10731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Martens C, Stein RA, Masureel M, Roth A, Mishra S, Dawaliby R, Konijnenberg A, Sobott F, Govaerts C, McHaourab HS (2016) Lipids modulate the conformational dynamics of a secondary multidrug transporter. Nat Struct Mol Biol 23(8):744–751. https://doi.org/10.1038/nsmb.3262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Fabre L, Bao H, Innes J, Duong F, Rouiller I (2017) Negative stain single-particle EM of the maltose transporter in nanodiscs reveals asymmetric closure of MalK2 and catalytic roles of ATP, MalE, and maltose. J Biol Chem 292(13):5457–5464. https://doi.org/10.1074/jbc.M116.757898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Zoghbi ME, Mok L, Swartz DJ, Singh A, Fendley GA, Urbatsch IL, Altenberg GA (2017) Substrate-induced conformational changes in the nucleotide-binding domains of lipid bilayer-associated P-glycoprotein during ATP hydrolysis. J Biol Chem 292(50):20412–20424. https://doi.org/10.1074/jbc.M117.814186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Orelle C, Durmort C, Mathieu K, Duchene B, Aros S, Fenaille F, Andre F, Junot C, Vernet T, Jault JM (2018) A multidrug ABC transporter with a taste for GTP. Sci Rep 8(1):2309. https://doi.org/10.1038/s41598-018-20558-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Dalal K, Duong F (2011) The SecY complex: conducting the orchestra of protein translocation. Trends Cell Biol 21(9):506–514. https://doi.org/10.1016/j.tcb.2011.04.005

    Article  CAS  PubMed  Google Scholar 

  73. Katayama H, Wang J, Tama F, Chollet L, Gogol EP, Collier RJ, Fisher MT (2010) Three-dimensional structure of the anthrax toxin pore inserted into lipid nanodiscs and lipid vesicles. Proc Natl Acad Sci U S A 107(8):3453–3457, S3453/3451–S3453/3453

    Article  CAS  Google Scholar 

  74. Wu Z, Auclair SM, Bello O, Vennekate W, Dudzinski NR, Krishnakumar SS, Karatekin E (2016) Nanodisc-cell fusion: control of fusion pore nucleation and lifetimes by SNARE protein transmembrane domains. Sci Rep 6:27287. https://doi.org/10.1038/srep27287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Bao H, Goldschen-Ohm M, Jeggle P, Chanda B, Edwardson JM, Chapman ER (2016) Exocytotic fusion pores are composed of both lipids and proteins. Nat Struct Mol Biol 23(1):67–73. https://doi.org/10.1038/nsmb.3141

    Article  CAS  PubMed  Google Scholar 

  76. Xu XP, Zhai D, Kim E, Swift M, Reed JC, Volkmann N, Hanein D (2013) Three-dimensional structure of Bax-mediated pores in membrane bilayers. Cell Death Dis 4(June):e683. https://doi.org/10.1038/cddis.2013.210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Gatsogiannis C, Merino F, Prumbaum D, Roderer D, Leidreiter F, Meusch D, Raunser S (2016) Membrane insertion of a Tc toxin in near-atomic detail. Nat Struct Mol Biol. https://doi.org/10.1038/nsmb.3281

  78. Akkaladevi N, Mukherjee S, Katayama H, Janowiak B, Patel D, Gogol EP, Pentelute BL, John Collier R, Fisher MT (2015) Following natures lead: on the construction of membrane-inserted toxins in lipid bilayer Nanodiscs. J Membr Biol 248(3):595–607. https://doi.org/10.1007/s00232-014-9768-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Meusch D, Gatsogiannis C, Efremov RG, Lang AE, Hofnagel O, Vetter IR, Aktories K, Raunser S (2014) Mechanism of Tc toxin action revealed in molecular detail. Nature 508(7494):61–65. https://doi.org/10.1038/nature13015

    Article  CAS  PubMed  Google Scholar 

  80. Boldog T, Grimme S, Li M, Sligar SG, Hazelbauer GL (2006) Nanodiscs separate chemoreceptor oligomeric states and reveal their signaling properties. Proc Natl Acad Sci U S A 103(31):11509–11514. https://doi.org/10.1073/pnas.0604988103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Li M, Hazelbauer GL (2011) Core unit of chemotaxis signaling complexes. Proc Natl Acad Sci U S A 108(23):9390–9395. https://doi.org/10.1073/pnas.1104824108

    Article  PubMed  PubMed Central  Google Scholar 

  82. Glueck JM, Koenig BW, Willbold D (2011) Nanodiscs allow the use of integral membrane proteins as analytes in surface plasmon resonance studies. Anal Biochem 408(1):46–52. https://doi.org/10.1016/j.ab.2010.08.028

    Article  CAS  Google Scholar 

  83. Mi L-Z, Grey MJ, Nishida N, Walz T, Lu C, Springer TA (2008) Functional and structural stability of the epidermal growth factor receptor in detergent micelles and phospholipid nanodiscs. Biochemistry 47(39):10314–10323

    Article  CAS  Google Scholar 

  84. Yoshiura C, Ueda T, Kofuku Y, Matsumoto M, Okude J, Kondo K, Shiraishi Y, Shimada I (2015) Elucidation of the CCR1- and CCR5-binding modes of MIP-1alpha by application of an NMR spectra reconstruction method to the transferred cross-saturation experiments. J Biomol NMR 63(4):333–340. https://doi.org/10.1007/s10858-015-9992-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Gutmann T, Kim KH, Grzybek M, Walz T, Coskun U (2018) Visualization of ligand-induced transmembrane signaling in the full-length human insulin receptor. J Cell Biol. https://doi.org/10.1083/jcb.201711047

  86. Bartelli NL, Hazelbauer GL (2016) Bacterial chemoreceptor dynamics: helical stability in the cytoplasmic domain varies with functional segment and adaptational modification. J Mol Biol 428(19):3789–3804. https://doi.org/10.1016/j.jmb.2016.06.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Eismann S, Endres RG (2015) Protein connectivity in chemotaxis receptor complexes. PLoS Comput Biol 11(12):e1004650

    Article  Google Scholar 

  88. Näsvik Öjemyr L, von Ballmoos C, Gennis RB, Sligar SG, Brzezinski P (2012) Reconstitution of respiratory oxidases in membrane nanodiscs for investigation of proton-coupled electron transfer. FEBS Lett. https://doi.org/10.1016/j.febslet.2011.12.023

  89. Bayburt TH, Leitz AJ, Xie G, Oprian DD, Sligar SG (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J Biol Chem 282(20):14875–14881. https://doi.org/10.1074/jbc.M701433200

    Article  CAS  PubMed  Google Scholar 

  90. Ranaghan MJ, Schwall CT, Alder NN, Birge RR (2011) Green proteorhodopsin reconstituted into nanoscale phospholipid bilayers (nanodiscs) as photoactive monomers. J Am Chem Soc 133(45):18318–18327. https://doi.org/10.1021/ja2070957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Boldog T, Li M, Hazelbauer GL (2007) Using Nanodiscs to create water-soluble transmembrane chemoreceptors inserted in lipid bilayers. Methods Enzymol 423:317–335

    Article  CAS  Google Scholar 

  92. Zhang XX, Chan CS, Bao H, Fang Y, Foster LJ, Duong F (2012) Nanodiscs and SILAC-based mass spectrometry to identify a membrane protein interactome. J Proteome Res 11(2):1454–1459. https://doi.org/10.1021/pr200846y

    Article  CAS  PubMed  Google Scholar 

  93. Baas BJ, Denisov IG, Sligar SG (2004) Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch Biochem Biophys 430(2):218–228. https://doi.org/10.1016/j.abb.2004.07.003

    Article  CAS  PubMed  Google Scholar 

  94. Denisov IG, Sligar SG (2011) Cytochromes P 450 in nanodisks. Biochim Biophys Acta Proteins Proteomics 1814(1):223–229. https://doi.org/10.1016/j.bbapap.2010.05.017

    Article  CAS  Google Scholar 

  95. Duan H, Civjan NR, Sligar SG, Schuler MA (2004) Co-incorporation of heterologously expressed Arabidopsis cytochrome P450 and P450 reductase into soluble nanoscale lipid bilayers. Arch Biochem Biophys 424(2):141–153. https://doi.org/10.1016/j.abb.2004.02.010

    Article  CAS  PubMed  Google Scholar 

  96. Duan H, Schuler MA (2006) Heterologous expression and strategies for encapsulation of membrane-localized plant P450s. Phytochem Rev 5(2–3):507–523

    Article  CAS  Google Scholar 

  97. Frank DJ, Denisov IG, Sligar SG (2011) Analysis of heterotropic cooperativity in cytochrome P450 3A4 using α-naphthoflavone and testosterone. J Biol Chem 286(7):5540–5545. https://doi.org/10.1074/jbc.M110.182055

    Article  CAS  PubMed  Google Scholar 

  98. Grinkova YV, Denisov IG, Sligar SG (2010) Functional reconstitution of monomeric CYP3A4 with multiple cytochrome P450 reductase molecules in Nanodiscs. Biochem Biophys Res Commun 398(2):194–198. https://doi.org/10.1016/j.bbrc.2010.06.058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Grinkova YV, Denisov IG, Waterman MR, Arase M, Kagawa N, Sligar SG (2008) The ferrous-oxy complex of human aromatase. Biochem Biophys Res Commun 372(2):379–382. https://doi.org/10.1016/j.bbrc.2008.05.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Morrissey JH, Pureza V, Davis-Harrison RL, Sligar SG, Ohkubo YZ, Tajkhorshid E (2008) Blood clotting reactions on nanoscale phospholipid bilayers. Thromb Res 122(Suppl 1):S23–S26. https://doi.org/10.1016/s0049-3848(08)70014-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Morrissey JH, Tajkhorshid E, Rienstra CM (2011) Nanoscale studies of protein-membrane interactions in blood clotting. J Thromb Haemost 9(Suppl 1):162–167. https://doi.org/10.1111/j.1538-7836.2011.04300.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Shaw AW, Pureza VS, Sligar SG, Morrissey JH (2007) The local phospholipid environment modulates the activation of blood clotting. J Biol Chem 282(9):6556–6563. https://doi.org/10.1074/jbc.M607973200

    Article  CAS  PubMed  Google Scholar 

  103. Tavoosi N, Davis-Harrison RL, Pogorelov TV, Ohkubo YZ, Arcario MJ, Clay MC, Rienstra CM, Tajkhorshid E, Morrissey JH (2011) Molecular determinants of phospholipid synergy in blood clotting. J Biol Chem 286(26):23247–23253. https://doi.org/10.1074/jbc.M111.251769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Bayburt TH, Grinkova YV, Sligar SG (2006) Assembly of single bacteriorhodopsin trimers in bilayer nanodiscs. Arch Biochem Biophys 450(2):215–222. https://doi.org/10.1016/j.abb.2006.03.013

    Article  CAS  PubMed  Google Scholar 

  105. Borch J, Roepstorff P, Moeller-Jensen J (2011) Nanodisc-based co-immunoprecipitation for mass spectrometric identification of membrane-interacting proteins. Mol Cell Proteomics 10(7):O110 006775, 006779. https://doi.org/10.1074/mcp.O110.006775

    Article  CAS  Google Scholar 

  106. Borch J, Torta F, Sligar SG, Roepstorff P (2008) Nanodiscs for immobilization of lipid bilayers and membrane receptors: kinetic analysis of cholera toxin binding to a glycolipid receptor. Anal Chem 80(16):6245–6252. https://doi.org/10.1021/ac8000644

    Article  CAS  PubMed  Google Scholar 

  107. Ahn T, Kim M, Yun CH, Chae HJ (2007) Functional regulation of hepatic cytochrome p450 enzymes by physicochemical properties of phospholipids in biological membranes. Curr Protein Pept Sci 8(5):496–505

    Article  CAS  Google Scholar 

  108. Shenkarev ZO, Lyukmanova EN, Solozhenkin OI, Gagnidze IE, Nekrasova OV, Chupin VV, Tagaev AA, Yakimenko ZA, Ovchinnikova TV, Kirpichnikov MP, Arseniev AS (2009) Lipid-protein nanodiscs: possible application in high-resolution NMR investigations of membrane proteins and membrane-active peptides. Biochem Mosc 74(7):756–765

    Article  CAS  Google Scholar 

  109. Zocher M, Roos C, Wegmann S, Bosshart PD, Dotsch V, Bernhard F, Muller DJ (2012) Single-molecule force spectroscopy from nanodiscs: an assay to quantify folding, stability, and interactions of native membrane proteins. ACS Nano 6(1):961–971. https://doi.org/10.1021/nn204624p

    Article  CAS  PubMed  Google Scholar 

  110. Morrissey JH, Pureza V, Davis-Harrison RL, Sligar SG, Rienstra CM, Kijac AZ, Ohkubo YZ, Tajkhorshid E (2009) Protein-membrane interactions: blood clotting on nanoscale bilayers. J Thromb Haemostasis 7(Suppl 1):169–172

    Article  CAS  Google Scholar 

  111. Kobashigawa Y, Harada K, Yoshida N, Ogura K, Inagaki F (2011) Phosphoinositide-incorporated lipid-protein nanodiscs: a tool for studying protein-lipid interactions. Anal Biochem 410(1):77–83. https://doi.org/10.1016/j.ab.2010.11.021

    Article  CAS  PubMed  Google Scholar 

  112. Boettcher JM, Davis-Harrison RL, Clay MC, Nieuwkoop AJ, Ohkubo YZ, Tajkhorshid E, Morrissey JH, Rienstra CM (2011) Atomic view of calcium-induced clustering of phosphatidylserine in mixed lipid bilayers. Biochemistry 50(12):2264–2273. https://doi.org/10.1021/bi1013694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Morrissey JH, Davis-Harrison RL, Tavoosi N, Ke K, Pureza V, Boettcher JM, Clay MC, Rienstra CM, Ohkubo YZ, Pogorelov TV, Tajkhorshid E (2010) Protein-Phospholipid interactions in blood clotting. Thromb Res 125(Suppl 1):S23–S25

    Article  CAS  Google Scholar 

  114. Trahey M, Li MJ, Kwon H, Woodahl EL, McClary WD, Atkins WM (2015) Applications of lipid Nanodiscs for the study of membrane proteins by surface plasmon resonance. Curr Protoc Protein Sci 81:29.13.1–29.13.16. https://doi.org/10.1002/0471140864.ps2913s81

    Article  Google Scholar 

  115. Marty MT, Sloan CD, Bailey RC, Sligar SG (2012) Nonlinear analyte concentration gradients for one-step kinetic analysis employing optical microring resonators. Anal Chem 84(13):5556–5564. https://doi.org/10.1021/ac300478f

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Das A, Zhao J, Schatz GC, Sligar SG, Van Duyne RP (2009) Screening of type I and II drug binding to human cytochrome P450-3A4 in nanodiscs by localized surface plasmon resonance spectroscopy. Anal Chem 81(10):3754–3759. https://doi.org/10.1021/ac802612z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Zhao J, Das A, Schatz GC, Sligar SG, Van Duyne RP (2008) Resonance localized surface plasmon spectroscopy: sensing substrate and inhibitor binding to cytochrome P450. J Phys Chem C 112(34):13084–13088

    Article  CAS  Google Scholar 

  118. Zhao J, Das A, Zhang XY, Schatz GC, Sligar SG, Van Duyne RP (2006) Resonance surface plasmon spectroscopy: low molecular weight substrate binding to cytochrome P450. J Am Chem Soc 128(34):11004–11005. https://doi.org/10.1021/ja0636082

    Article  CAS  PubMed  Google Scholar 

  119. Sloan CD, Marty MT, Sligar SG, Bailey RC (2013) Interfacing lipid bilayer nanodiscs and silicon photonic sensor arrays for multiplexed protein-lipid and protein-membrane protein interaction screening. Anal Chem 85(5):2970–2976. https://doi.org/10.1021/ac3037359

    Article  CAS  PubMed  Google Scholar 

  120. Ye X, McLean MA, Sligar SG (2016) Conformational equilibrium of talin is regulated by anionic lipids. Biochim Biophys Acta 1858(8):1833–1840. https://doi.org/10.1016/j.bbamem.2016.05.005

    Article  CAS  PubMed  Google Scholar 

  121. Lam Q, Kato M, Cheruzel L (2016) Ru(II)-diimine functionalized metalloproteins: from electron transfer studies to light-driven biocatalysis. Biochim Biophys Acta 1857(5):589–597. https://doi.org/10.1016/j.bbabio.2015.09.004

    Article  CAS  PubMed  Google Scholar 

  122. Scott JR, Willie A, McLean M, Stayton PS, Sligar SG, Durham B, Millett F (1993) Intramolecular electron transfer in cytochrome b5 labeled with ruthenium(II) polypyridine complexes: rate measurements in the Marcus inverted region. J Am Chem Soc 115(15):6820–6824. https://doi.org/10.1021/ja00068a045

    Article  CAS  Google Scholar 

  123. Gregory MC, McLean MA, Sligar SG (2017) Interaction of KRas4b with anionic membranes: a special role for PIP2. Biochem Biophys Res Commun 487(2):351–355. https://doi.org/10.1016/j.bbrc.2017.04.063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Hagn F, Nasr ML, Wagner G (2018) Assembly of phospholipid nanodiscs of controlled size for structural studies of membrane proteins by NMR. Nat Protoc 13(1):79–98. https://doi.org/10.1038/nprot.2017.094

    Article  CAS  PubMed  Google Scholar 

  125. Mazhab-Jafari MT, Marshall CB, Smith MJ, Gasmi-Seabrook GM, Stathopulos PB, Inagaki F, Kay LE, Neel BG, Ikura M (2015) Oncogenic and RASopathy-associated K-RAS mutations relieve membrane-dependent occlusion of the effector-binding site. Proc Natl Acad Sci U S A 112(21):6625–6630. https://doi.org/10.1073/pnas.1419895112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Xu L, Ojemyr LN, Bergstrand J, Brzezinski P, Widengren J (2016) Protonation dynamics on lipid nanodiscs: influence of the membrane surface area and external buffers. Biophys J 110(9):1993–2003. https://doi.org/10.1016/j.bpj.2016.03.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Sanden T, Salomonsson L, Brzezinski P, Widengren J (2010) Surface-coupled proton exchange of a membrane-bound proton acceptor. Proc Natl Acad Sci U S A 107(9):4129–4134. https://doi.org/10.1073/pnas.0908671107

    Article  PubMed  PubMed Central  Google Scholar 

  128. Li MJ, Guttman M, Atkins WM (2018) Conformational dynamics of P-glycoprotein in lipid nanodiscs and detergent micelles reveal complex motions on a wide time scale. J Biol Chem. https://doi.org/10.1074/jbc.RA118.002190

  129. Treuheit NA, Redhair M, Kwon H, McClary WD, Guttman M, Sumida JP, Atkins WM (2016) Membrane interactions, ligand-dependent dynamics, and stability of cytochrome P4503A4 in lipid nanodiscs. Biochemistry 55(7):1058–1069. https://doi.org/10.1021/acs.biochem.5b01313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95(11):6448–6453

    Article  CAS  Google Scholar 

  131. Wilcox K, Lacor P, Pitt J, Klein W (2011) Abeta oligomer-induced synapse degeneration in Alzheimer’s disease. Cell Mol Neurobiol 31(6):939–948. https://doi.org/10.1007/s10571-011-9691-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Miwa GT, Lu AY (1981) Studies on the stimulation of cytochrome P-450-dependent monooxygenase activity by dilauroylphosphatidylcholine. Arch Biochem Biophys 211(1):454–458

    Article  CAS  Google Scholar 

  133. Imaoka S, Imai Y, Shimada T, Funae Y (1992) Role of phospholipids in reconstituted cytochrome P450 3A form and mechanism of their activation of catalytic activity. Biochemistry 31(26):6063–6069

    Article  CAS  Google Scholar 

  134. Kim KH, Ahn T, Yun CH (2003) Membrane properties induced by anionic phospholipids and phosphatidylethanolamine are critical for the membrane binding and catalytic activity of human cytochrome P450 3A4. Biochemistry 42(51):15377–15387. https://doi.org/10.1021/bi035280k

    Article  CAS  PubMed  Google Scholar 

  135. Gajsiewicz JM, Morrissey JH (2015) Structure-function relationship of the interaction between tissue factor and factor VIIa. Semin Thromb Hemost 41(7):682–690. https://doi.org/10.1055/s-0035-1564044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Muehl EM, Gajsiewicz JM, Medfisch SM, Wiersma ZSB, Morrissey JH, Bailey RC (2017) Multiplexed silicon photonic sensor arrays enable facile characterization of coagulation protein binding to nanodiscs with variable lipid content. J Biol Chem 292(39):16249–16256. https://doi.org/10.1074/jbc.M117.800938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Grinkova YV, Denisov IG, McLean MA, Sligar SG (2013) Oxidase uncoupling in heme monooxygenases: human cytochrome P450 CYP3A4 in Nanodiscs. Biochem Biophys Res Commun 430(4):1223–1227. https://doi.org/10.1016/j.bbrc.2012.12.072

    Article  CAS  PubMed  Google Scholar 

  138. Malhotra K, Alder NN (2014) Advances in the use of nanoscale bilayers to study membrane protein structure and function. Biotechnol Genet Eng Rev 30(1):79–93. https://doi.org/10.1080/02648725.2014.921502

    Article  CAS  PubMed  Google Scholar 

  139. Szundi I, Funatogawa C, Guo Y, Yan ECY, Kliger DS (2017) Protein sequence and membrane lipid roles in the activation kinetics of bovine and human rhodopsins. Biophys J. https://doi.org/10.1016/j.bpj.2017.08.051

  140. Van Eps N, Caro LN, Morizumi T, Kusnetzow AK, Szczepek M, Hofmann KP, Bayburt TH, Sligar SG, Ernst OP, Hubbell WL (2017) Conformational equilibria of light-activated rhodopsin in nanodiscs. Proc Natl Acad Sci U S A 114(16):E3268–E3275. https://doi.org/10.1073/pnas.1620405114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Marty MT, Das A, Sligar SG (2012) Ultra-thin layer MALDI mass spectrometry of membrane proteins in nanodiscs. Anal Bioanal Chem 402(2):721–729. https://doi.org/10.1007/s00216-011-5512-3

    Article  CAS  PubMed  Google Scholar 

  142. Zoghbi ME, Cooper RS, Altenberg GA (2016) The lipid bilayer modulates the structure and function of an ATP-binding cassette exporter. J Biol Chem 291(9):4453–4461. https://doi.org/10.1074/jbc.M115.698498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Yokogawa M, Kobashigawa Y, Yoshida N, Ogura K, Harada K, Inagaki F (2012) NMR analyses of the interaction between the FYVE domain of early endosome antigen 1 (EEA1) and phosphoinositide embedded in a lipid bilayer. J Biol Chem 287(42):34936–34945. https://doi.org/10.1074/jbc.M112.398255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Wan C, Wu B, Song Z, Zhang J, Chu H, Wang A, Liu Q, Shi Y, Li G, Wang J (2015) Insights into the molecular recognition of the granuphilin C2A domain with PI(4,5)P2. Chem Phys Lipids 186:61–67. https://doi.org/10.1016/j.chemphyslip.2015.01.003

    Article  CAS  PubMed  Google Scholar 

  145. Efremov RG, Gatsogiannis C, Raunser S (2017) Lipid nanodiscs as a tool for high-resolution structure determination of membrane proteins by single-particle cryo-EM. Methods Enzymol 594:1–30. https://doi.org/10.1016/bs.mie.2017.05.007

    Article  CAS  PubMed  Google Scholar 

  146. Mi W, Li Y, Yoon SH, Ernst RK, Walz T, Liao M (2017) Structural basis of MsbA-mediated lipopolysaccharide transport. Nature 549(7671):233–237. https://doi.org/10.1038/nature23649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Dai A, Ye F, Taylor DW, Hu G, Ginsberg MH, Taylor KA (2015) The structure of a full-length membrane-embedded integrin bound to a physiological ligand. J Biol Chem 290(45):27168–27175. https://doi.org/10.1074/jbc.M115.682377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Xu X-P, Kim E, Swift M, Smith JW, Volkmann N, Hanein D (2016) Three-dimensional structures of full-length, membrane-embedded human αIIbβ3 integrin complexes. Biophys J 110(4):798–809. https://doi.org/10.1016/j.bpj.2016.01.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Hanein D, Volkmann N (2018) Conformational equilibrium of human platelet integrin investigated by three-dimensional electron cryo-microscopy. Subcell Biochem 87:353–363. https://doi.org/10.1007/978-981-10-7757-9_12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Grushin K, Miller J, Dalm D, Stoilova-McPhie S (2015) Factor VIII organisation on nanodiscs with different lipid composition. Thromb Haemost 113(4):741–749. https://doi.org/10.1160/th14-09-0725

    Article  PubMed  Google Scholar 

  151. Stoilova-McPhie S, Grushin K, Dalm D, Miller J (2014) Lipid nanotechnologies for structural studies of membrane-associated proteins. Proteins 82(11):2902–2909. https://doi.org/10.1002/prot.24631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Lee H, Shingler KL, Organtini LJ, Ashley RE, Makhov AM, Conway JF, Hafenstein S (2016) The novel asymmetric entry intermediate of a picornavirus captured with nanodiscs. Sci Adv 2(8):e1501929. https://doi.org/10.1126/sciadv.1501929

    Article  PubMed  PubMed Central  Google Scholar 

  153. Popot JL (2010) Amphipols, nanodiscs, and fluorinated surfactants: three nonconventional approaches to studying membrane proteins in aqueous solutions. Annu Rev Biochem 79:737–775. https://doi.org/10.1146/annurev.biochem.052208.114057

    Article  CAS  PubMed  Google Scholar 

  154. Raschle T, Hiller S, Etzkorn M, Wagner G (2010) Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr Opin Struct Biol 20(4):471–479. https://doi.org/10.1016/j.sbi.2010.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Serebryany E, Zhu GA, Yan ECY (2012) Artificial membrane-like environments for in vitro studies of purified G-protein coupled receptors. Biochim Biophys Acta Biomembr 1818(2):225–233. https://doi.org/10.1016/j.bbamem.2011.07.047

    Article  CAS  Google Scholar 

  156. Ravula T, Ramadugu SK, Di Mauro G, Ramamoorthy A (2017) Bioinspired, size-tunable self-assembly of polymer-lipid bilayer nanodiscs. Angew Chem Int Ed 56(38):11466–11470. https://doi.org/10.1002/anie.201705569

    Article  CAS  Google Scholar 

  157. Yasuhara K, Arakida J, Ravula T, Ramadugu SK, Sahoo B, Kikuchi J-i, Ramamoorthy A (2017) Spontaneous lipid nanodisc formation by amphiphilic polymethacrylate copolymers. J Am Chem Soc 139(51):18657–18663. https://doi.org/10.1021/jacs.7b10591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Laursen T, Borch J, Knudsen C, Bavishi K, Torta F, Martens HJ, Silvestro D, Hatzakis NS, Wenk MR, Dafforn TR, Olsen CE, Motawia MS, Hamberger B, Moller BL, Bassard J-E (2016) Characterization of a dynamic metabolon producing the defense compound dhurrin in sorghum. Science 354(6314):890–893. https://doi.org/10.1126/science.aag2347

    Article  CAS  PubMed  Google Scholar 

  159. Parmar M, Rawson S, Scarff CA, Goldman A, Dafforn TR, Muench SP, Postis VLG (2018) Using a SMALP platform to determine a sub-nm single particle cryo-EM membrane protein structure. Biochim Biophys Acta 1860(2):378–383. https://doi.org/10.1016/j.bbamem.2017.10.005

    Article  CAS  PubMed Central  Google Scholar 

  160. Flayhan A, Mertens HDT, Ural-Blimke Y, Martinez Molledo M, Svergun DI, Loew C (2018) Saposin lipid nanoparticles: a highly versatile and modular tool for membrane protein research. Structure 26(2):345–355.e345. https://doi.org/10.1016/j.str.2018.01.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Shenkarev ZO, Lyukmanova EN, Paramonov AS, Panteleev PV, Balandin SV, Shulepko MA, Mineev KS, Ovchinnikova TV, Kirpichnikov MP, Arseniev AS (2014) Lipid-protein nanodiscs offer new perspectives for structural and functional studies of water-soluble membrane-active peptides. Acta Nat 6(2):84–94

    Article  CAS  Google Scholar 

  162. Rues R-B, Henrich E, Boland C, Caffrey M, Bernhard F (2016) Cell-free production of membrane proteins in Escherichia coli lysates for functional and structural studies. Methods Mol Biol 1432:1–21. https://doi.org/10.1007/978-1-4939-3637-3_1

    Article  CAS  PubMed  Google Scholar 

  163. Viegas A, Viennet T, Etzkorn M (2016) The power, pitfalls and potential of the nanodisc system for NMR-based studies. Biol Chem 397(12):1335–1354. https://doi.org/10.1515/hsz-2016-0224

    Article  CAS  PubMed  Google Scholar 

  164. Puthenveetil R, Nguyen K, Vinogradova O (2017) Nanodiscs and solution NMR: preparation, application and challenges. Nanotechnol Rev 6(1):111–126. https://doi.org/10.1515/ntrev-2016-0076

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by National Institutes of Health through a MIRA grant R35-GM118145 to S.G.S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen G. Sligar .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Denisov, I.G., Schuler, M.A., Sligar, S.G. (2019). Nanodiscs as a New Tool to Examine Lipid–Protein Interactions. In: Kleinschmidt, J. (eds) Lipid-Protein Interactions. Methods in Molecular Biology, vol 2003. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-9512-7_25

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-9512-7_25

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-4939-9511-0

  • Online ISBN: 978-1-4939-9512-7

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics