Skip to main content

Lateral Diffusion in Heterogeneous Cell Membranes

  • Chapter
  • First Online:
Physics of Biological Membranes

Abstract

The plasma membrane is organized at numerous levels as a result of its large variety of molecular constituents and of selective interactions between them. Lateral diffusion, a direct physical consequence of the Brownian agitation, plays a key organizational role by constantly redistributing the membrane constituents among the possible molecular associations. In this context, we will first review the physical mechanisms contributing to the creation of inhomogeneity. We will then describe the current methodological approaches allowing us to measure diffusion in living cells. The different levels of membrane organization will be discussed before illustrating the impact of the dynamic organization of the membrane on cellular functions.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 299.99
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. Engelman DM (2005) Membranes are more mosaic than fluid. Nature 438:578–580

    Article  CAS  PubMed  Google Scholar 

  2. Jacobson K, Sheets ED, Simson R (1995) Revisiting the fluid mosaic model of membranes. Science 268:1441–1442

    Article  CAS  PubMed  Google Scholar 

  3. Kusumi A, Suzuki KG, Kasai RS, Ritchie K, Fujiwara TK (2011) Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 36:604–615

    Article  CAS  PubMed  Google Scholar 

  4. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572

    Article  CAS  PubMed  Google Scholar 

  5. Nicolson GL (2014) The Fluid-Mosaic Model of Membrane Structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochim Biophys Acta 1838:1451–1466

    Article  CAS  PubMed  Google Scholar 

  6. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731

    Article  CAS  PubMed  Google Scholar 

  7. Axelrod D, Koppel DE, Schlessinger J, Elson E, Webb WW (1976) Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J 16:1055–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Barak LS, Webb WW (1982) Diffusion of low density lipoprotein-receptor complex on human fibroblasts. J Cell Biol 95:846–852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Koppel DE, Axelrod D, Schlessinger J, Elson EL, Webb WW (1976) Dynamics of fluorescence marker concentration as a probe of mobility. Biophys J 16:1315–1329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Frye LD, Edidin M (1970) The rapid intermixing of cell surface antigens after formation of mouse-human heterokaryons. J Cell Sci 7:319–335

    CAS  PubMed  Google Scholar 

  11. Mouritsen OG, Bagatolli LA (2016) Life—as a matter of fat. Springer, Heidelberg

    Book  Google Scholar 

  12. Marguet D, Lenne PF, Rigneault H, He HT (2006) Dynamics in the plasma membrane: how to combine fluidity and order. EMBO J 25:3446–3457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Shinbrot T, Muzzio FJ (2001) Noise to order. Nature 410:251–258

    Article  CAS  PubMed  Google Scholar 

  14. Yanagida T, Ueda M, Murata T, Esaki S, Ishii Y (2007) Brownian motion, fluctuation and life. Bio Systems 88:228–242

    Article  CAS  PubMed  Google Scholar 

  15. Prior IA, Muncke C, Parton RG, Hancock JF (2003) Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Biol 160:165–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Van Zanten TS, Gomez J, Manzo C, Cambi A, Buceta J, Reigada R, Garcia-Parajo MF (2010) Direct mapping of nanoscale compositional connectivity on intact cell membranes. Proc Natl Acad Sci USA 107:15437–15442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Takatori S, Mesman R, Fujimoto T (2014) Microscopic methods to observe the distribution of lipids in the cellular membrane. Biochemistry 53:639–653

    Article  CAS  PubMed  Google Scholar 

  18. Tanaka KA, Suzuki KG, Shirai YM, Shibutani ST, Miyahara MS, Tsuboi H, Yahara M, Yoshimura A, Mayor S, Fujiwara TK, Kusumi A (2010) Membrane molecules mobile even after chemical fixation. Nat Methods 7:865–866

    Article  CAS  PubMed  Google Scholar 

  19. Magde D, Elson EL, Webb WW (1974) Fluorescence correlation spectroscopy. II. An experimental realization. Biopolymers 13:29–61

    Article  CAS  PubMed  Google Scholar 

  20. Bacia K, Kim SA, Schwille P (2006) Fluorescence cross-correlation spectroscopy in living cells. Nat Methods 3:83–89

    Article  CAS  PubMed  Google Scholar 

  21. Arnspang EC, Schwartzentruber J, Clausen MP, Wiseman PW, Lagerholm BC (2013) Bridging the gap between single molecule and ensemble methods for measuring lateral dynamics in the plasma membrane. PLoS One 8:e78096

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Curthoys NM, Parent M, Mlodzianoski M, Nelson AJ, Lilieholm J, Butler MB, Valles M, Hess ST (2015) Dances with membranes: breakthroughs from super-resolution imaging. Curr Top Membr 75:59–123

    Article  PubMed  PubMed Central  Google Scholar 

  23. Blumenthal D, Goldstien L, Edidin M, Gheber LA (2015) Universal approach to FRAP analysis of arbitrary bleaching patterns. Sci Rep 5:11655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Tetin SY (2013) Methods in enzymology. Fluorescence fluctuation spectroscopy (FFS), part A. Preface. Methods Enzymol 518:xi–xii

    Article  PubMed  Google Scholar 

  25. Tetin SY (2013) Methods in enzymology. Fluorescence fluctuation spectroscopy (FFS), part B. Preface. Methods Enzymol 519:xiii–xxiv

    Article  PubMed  Google Scholar 

  26. Garcia-Parajo MF, Cambi A, Torreno-Pina JA, Thompson N, Jacobson K (2014) Nanoclustering as a dominant feature of plasma membrane organization. J Cell Sci 127:4995–5005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Yechiel E, Edidin M (1987) Micrometer-scale domains in fibroblast plasma membranes. J Cell Biol 105:755–760

    Article  CAS  PubMed  Google Scholar 

  28. Baker AM, Sauliere A, Gaibelet G, Lagane B, Mazeres S, Fourage M, Bachelerie F, Salome L, Lopez A, Dumas F (2007) CD4 interacts constitutively with multiple CCR5 at the plasma membrane of living cells. A fluorescence recovery after photobleaching at variable radii approach. J Biol Chem 282:35163–35168

    Article  CAS  PubMed  Google Scholar 

  29. Pucadyil TJ, Chattopadhyay A (2007) Cholesterol depletion induces dynamic confinement of the G-protein coupled serotonin(1A) receptor in the plasma membrane of living cells. Biochim Biophys Acta 1768:655–668

    Article  CAS  PubMed  Google Scholar 

  30. Salome L, Cazeils JL, Lopez A, Tocanne JF (1998) Characterization of membrane domains by FRAP experiments at variable observation areas. Eur Biophys J 27:391–402

    Article  CAS  PubMed  Google Scholar 

  31. Sauliere-Nzeh Ndong A, Millot C, Corbani M, Mazeres S, Lopez A, Salome L (2010) Agonist-selective dynamic compartmentalization of human Mu opioid receptor as revealed by resolutive FRAP analysis. J Biol Chem 285:14514–14520

    Article  PubMed  CAS  Google Scholar 

  32. Lenne PF, Wawrezinieck L, Conchonaud F, Wurtz O, Boned A, Guo XJ, Rigneault H, He HT, Marguet D (2006) Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J 25:3245–3256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wawrezinieck L, Rigneault H, Marguet D, Lenne PF (2005) Fluorescence correlation spectroscopy diffusion laws to probe the submicron cell membrane organization. Biophys J 89:4029–4042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wenger J, Conchonaud F, Dintinger J, Wawrezinieck L, Ebbesen TW, Rigneault H, Marguet D, Lenne PF (2007) Diffusion analysis within single nanometric apertures reveals the ultrafine cell membrane organization. Biophys J 92:913–919

    Article  CAS  PubMed  Google Scholar 

  35. Vicidomini G, Ta H, Honigmann A, Mueller V, Clausen MP, Waithe D, Galiani S, Sezgin E, Diaspro A, Hell SW, Eggeling C (2015) STED-FLCS: an advanced tool to reveal spatiotemporal heterogeneity of molecular membrane dynamics. Nano Lett 15:5912–5918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Meilhac N, Le Guyader L, Salome L, Destainville N (2006) Detection of confinement and jumps in single-molecule membrane trajectories. Phys Rev E Stat Nonlin Soft Matter Phys 73:011915

    Article  CAS  PubMed  Google Scholar 

  37. Serge A, Bertaux N, Rigneault H, Marguet D (2008) Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes. Nat Methods 5:687–694

    Article  CAS  PubMed  Google Scholar 

  38. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157:1071–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Masson JB, Casanova D, Turkcan S, Voisinne G, Popoff MR, Vergassola M, Alexandrou A (2009) Inferring maps of forces inside cell membrane microdomains. Phys Rev Lett 102:048103

    Article  PubMed  CAS  Google Scholar 

  40. Turkcan S, Alexandrou A, Masson JB (2012) A Bayesian inference scheme to extract diffusivity and potential fields from confined single-molecule trajectories. Biophys J 102:2288–2298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. El Beheiry M, Dahan M, Masson JB (2015) InferenceMAP: mapping of single-molecule dynamics with Bayesian inference. Nat Methods 12:594–595

    Article  CAS  PubMed  Google Scholar 

  42. Destainville N, Salome L (2006) Quantification and correction of systematic errors due to detector time-averaging in single-molecule tracking experiments. Biophys J 90:L17–L19

    Article  CAS  PubMed  Google Scholar 

  43. Haanappel E, Mascalchi P, Carayon K, Mazères S, Salomé L (2012) Probing the influence of the particle in Single Particle Tracking measurements of lipid diffusion. Soft Matter 8:4462–4470

    Article  CAS  Google Scholar 

  44. Dragsten P, Henkart P, Blumenthal R, Weinstein J, Schlessinger J (1979) Lateral diffusion of surface immunoglobulin, Thy-1 antigen, and a lipid probe in lymphocyte plasma membranes. Proc Natl Acad Sci USA 76:5163–5167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wolf DE, Handyside AH, Edidin M (1982) Effect of microvilli on lateral diffusion measurements made by the fluorescence photobleaching recovery technique. Biophys J 38:295–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Adler J, Shevchuk AI, Novak P, Korchev YE, Parmryd I (2010) Plasma membrane topography and interpretation of single-particle tracks. Nat Methods 7:170–171

    Article  CAS  PubMed  Google Scholar 

  47. Kusters R, Storm C (2014) Impact of morphology on diffusive dynamics on curved surfaces. Phys Rev E Stat Nonlin Soft Matter Phys 89:032723

    Article  PubMed  CAS  Google Scholar 

  48. Parmryd I, Onfelt B (2013) Consequences of membrane topography. FEBS J 280:2775–2784

    Article  CAS  PubMed  Google Scholar 

  49. Jalink K, Van Rheenen J (2010) Nano-imaging of membrane topography affects interpretations in cell biology. Nat Methods 7:486

    Article  CAS  PubMed  Google Scholar 

  50. van Rheenen J, Jalink K (2002) Agonist-induced PIP(2) hydrolysis inhibits cortical actin dynamics: regulation at a global but not at a micrometer scale. Mol Biol Cell 13:3257–3267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Hall D (2008) Analysis and interpretation of two-dimensional single-particle tracking microscopy measurements: effect of local surface roughness. Anal Biochem 377:24–32

    Article  CAS  PubMed  Google Scholar 

  52. Abrahamsson S, Chen J, Hajj B, Stallinga S, Katsov AY, Wisniewski J, Mizuguchi G, Soule P, Mueller F, Dugast Darzacq C, Darzacq X, WU C, Bargmann CI, Agard DA, Dahan M, Gustafsson MG (2013) Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Nat Methods 10:60–63

    Article  CAS  PubMed  Google Scholar 

  53. Wells NP, Lessard GA, Phipps ME, Goodwin PM, Lidke DS, Wilson BS, Werner JH (2009) Going beyond 2D: Following membrane diffusion and topography in the IgE-Fc[Epsilon]RI system using 3-dimensional tracking microscopy. Proc SPIE Int Soc Opt Eng 7185:71850Z

    PubMed  PubMed Central  Google Scholar 

  54. Cognet L, Tardin C, Negrier ML, Breillat C, Coussen F, Choquet D, Lounis B (2008) Robust single-molecule approach for counting autofluorescent proteins. J Biomed Opt 13:031216

    Article  PubMed  CAS  Google Scholar 

  55. Low-Nam ST, Lidke KA, Cutler PJ, Roovers RC, van Bergen en Henegouwen PM, Wilson BS, Lidke DS (2011) ErbB1 dimerization is promoted by domain co-confinement and stabilized by ligand binding. Nat Struct Mol Biol 18:1244–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Digman MA, Dalal R, Horwitz AF, Gratton E (2008) Mapping the number of molecules and brightness in the laser scanning microscope. Biophys J 94:2320–2332

    Article  CAS  PubMed  Google Scholar 

  57. Chung I, Akita R, Vandlen R, Toomre D, Schlessinger J, Mellman I (2010) Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 464:783–787

    Article  CAS  PubMed  Google Scholar 

  58. Moriki T, Maruyama H, Maruyama IN (2001) Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain. J Mol Biol 311:1011–1026

    Article  CAS  PubMed  Google Scholar 

  59. Nagy P, Claus J, Jovin TM, Arndt-Jovin DJ (2010) Distribution of resting and ligand-bound ErbB1 and ErbB2 receptor tyrosine kinases in living cells using number and brightness analysis. Proc Natl Acad Sci USA 107:16524–16529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Saffarian S, Li Y, Elson EL, Pike LJ (2007) Oligomerization of the EGF receptor investigated by live cell fluorescence intensity distribution analysis. Biophys J 93:1021–1031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kozer N, Barua D, Henderson C, Nice EC, Burgess AW, Hlavacek WS, Clayton AH (2014) Recruitment of the adaptor protein Grb2 to EGFR tetramers. Biochemistry 53:2594–2604

    Article  CAS  PubMed  Google Scholar 

  62. Destainville N (2008) Cluster phases of membrane proteins. Phys Rev E Stat Nonlin Soft Matter Phys 77:011905

    Article  PubMed  CAS  Google Scholar 

  63. Meilhac N, Destainville N (2011) Clusters of proteins in biomembranes: insights into the roles of interaction potential shapes and of protein diversity. J Phys Chem B 115:7190–7199

    Article  CAS  PubMed  Google Scholar 

  64. Lajoie P, Partridge EA, Guay G, Goetz JG, Pawling J, Lagana A, Joshi B, Dennis JW, Nabi IR (2007) Plasma membrane domain organization regulates EGFR signaling in tumor cells. J Cell Biol 179:341–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Niemela PS, Miettinen MS, Monticelli L, Hammaren H, Bjelkmar P, Murtola T, Lindahl E, Vattulainen I (2010) Membrane proteins diffuse as dynamic complexes with lipids. J Am Chem Soc 132:7574–7575

    Article  CAS  PubMed  Google Scholar 

  66. Anderson RG, Jacobson K (2002) A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296:1821–1825

    Article  CAS  PubMed  Google Scholar 

  67. Elson EL, Fried E, Dolbow JE, Genin GM (2010) Phase separation in biological membranes: integration of theory and experiment. Annu Rev Biophys 39:207–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50

    Article  CAS  PubMed  Google Scholar 

  69. Sevcsik E, Schutz GJ (2016) With or without rafts? Alternative views on cell membranes. Bioessays 38:129–139

    Article  CAS  PubMed  Google Scholar 

  70. Ringerike T, Blystad FD, Levy FO, Madshus IH, Stang E (2002) Cholesterol is important in control of EGF receptor kinase activity but EGF receptors are not concentrated in caveolae. J Cell Sci 115:1331–1340

    CAS  PubMed  Google Scholar 

  71. Orr G, Hu D, Ozcelik S, Opresko LK, Wiley HS, Colson SD (2005) Cholesterol dictates the freedom of EGF receptors and HER2 in the plane of the membrane. Biophys J 89:1362–1373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ariotti N, Liang H, Xu Y, Zhang Y, Yonekubo Y, Inder K, Du G, Parton RG, Hancock JF, Plowman SJ (2010) Epidermal growth factor receptor activation remodels the plasma membrane lipid environment to induce nanocluster formation. Mol Cell Biol 30:3795–3804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Lambert S, Vind-Kezunovic D, Karvinen S, Gniadecki R (2006) Ligand-independent activation of the EGFR by lipid raft disruption. J Invest Dermatol 126:954–962

    Article  CAS  PubMed  Google Scholar 

  74. Rangamani P, Lipshtat A, Azeloglu EU, Calizo RC, Hu M, Ghassemi S, Hone J, Scarlata S, Neves SR, Iyengar R (2013) Decoding information in cell shape. Cell 154:1356–1369

    Article  CAS  PubMed  Google Scholar 

  75. Schmick M, Bastiaens PI (2014) The interdependence of membrane shape and cellular signal processing. Cell 156:1132–1138

    Article  CAS  PubMed  Google Scholar 

  76. Bigay J, Antonny B (2012) Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev Cell 23:886–895

    Article  CAS  PubMed  Google Scholar 

  77. Mcmahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590–596

    Article  CAS  PubMed  Google Scholar 

  78. Larsen JB, Jensen MB, Bhatia VK, Pedersen SL, Bjornholm T, Iversen L, Uline M, Szleifer I, Jensen KJ, Hatzakis NS, Stamou D (2015) Membrane curvature enables N-Ras lipid anchor sorting to liquid-ordered membrane phases. Nat Chem Biol 11:192–194

    Article  CAS  PubMed  Google Scholar 

  79. Reis P, Holmberg K, Watzke H, Leser ME, Miller R (2009) Lipases at interfaces: a review. Adv Colloid Interf Sci 147-148:237–250

    Article  CAS  Google Scholar 

  80. Windschiegl B, Orth A, Romer W, Berland L, Stechmann B, Bassereau P, Johannes L, Steinem C (2009) Lipid reorganization induced by Shiga toxin clustering on planar membranes. PLoS One 4:e6238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Simunovic M, Voth GA, Callan-Jones A, Bassereau P (2015) When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol 25:780–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Destainville N, Schmidt TH, Lang T (2016) Where biology meets physics-a converging view on membrane microdomain dynamics. Curr Top Membr 77:27–65

    Article  PubMed  Google Scholar 

  83. Saha S, Anilkumar AA, Mayor S (2016) GPI-anchored protein organization and dynamics at the cell surface. J Lipid Res 57:159–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Zhou Y, Hancock JF (2015) Ras nanoclusters: Versatile lipid-based signaling platforms. Biochim Biophys Acta 1853:841–849

    Article  CAS  PubMed  Google Scholar 

  85. Bethani I, Skanland SS, Dikic I, Acker-Palmer A (2010) Spatial organization of transmembrane receptor signalling. EMBO J 29:2677–2688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Saka SK, Honigmann A, Eggeling C, Hell SW, Lang T, Rizzoli SO (2014) Multi-protein assemblies underlie the mesoscale organization of the plasma membrane. Nat Commun 5:4509

    Article  CAS  PubMed  Google Scholar 

  87. Rys JP, Dufort CC, Monteiro DA, Baird MA, Oses-Prieto JA, Chand S, Burlingame AL, Davidson MW, Alliston TN (2015) Discrete spatial organization of TGFbeta receptors couples receptor multimerization and signaling to cellular tension. eLife 4:e09300

    Article  PubMed  PubMed Central  Google Scholar 

  88. Choudhuri K, Dustin ML (2010) Signaling microdomains in T cells. FEBS Lett 584:4823–4831

    Article  CAS  PubMed  Google Scholar 

  89. He HT, Marguet D (2008) T-cell antigen receptor triggering and lipid rafts: a matter of space and time scales. Talking Point on the involvement of lipid rafts in T-cell activation. EMBO Rep 9:525–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Huppa JB, Davis MM (2013) The interdisciplinary science of T-cell recognition. Adv Immunol 119:1–50

    Article  CAS  PubMed  Google Scholar 

  91. Klasener K, Maity PC, Hobeika E, Yang J, Reth M (2014) B cell activation involves nanoscale receptor reorganizations and inside-out signaling by Syk. eLife 3:e02069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Daumas F, Destainville N, Millot C, Lopez A, Dean D, Salome L (2003) Confined diffusion without fences of a g-protein-coupled receptor as revealed by single particle tracking. Biophys J 84:356–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Suzuki K, Ritchie K, Kajikawa E, Fujiwara T, Kusumi A (2005) Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques. Biophys J 88:3659–3680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Baker A, Sauliere A, Dumas F, Millot C, Mazeres S, Lopez A, Salome L (2007) Functional membrane diffusion of G-protein coupled receptors. Eur Biophys J 36:849–860

    Article  CAS  PubMed  Google Scholar 

  95. Veya L, Piguet J, Vogel H (2015) Single molecule imaging deciphers the relation between mobility and signaling of a prototypical G protein-coupled receptor in living cells. J Biol Chem 290:27723–27735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Pucadyil TJ, Kalipatnapu S, Harikumar KG, Rangaraj N, Karnik SS, Chattopadhyay A (2004) G-protein-dependent cell surface dynamics of the human serotonin1A receptor tagged to yellow fluorescent protein. Biochemistry 43:15852–15862

    Article  CAS  PubMed  Google Scholar 

  97. Carayon K, Mouledous L, Combedazou A, Mazeres S, Haanappel E, Salome L, Mollereau C (2014) Heterologous regulation of Mu-opioid (MOP) receptor mobility in the membrane of SH-SY5Y cells. J Biol Chem 289:28697–28706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Willig KI, Barrantes FJ (2014) Recent applications of superresolution microscopy in neurobiology. Curr Opin Chem Biol 20:16–21

    Article  CAS  PubMed  Google Scholar 

  99. Choquet D, Triller A (2013) The dynamic synapse. Neuron 80:691–703

    Article  CAS  PubMed  Google Scholar 

  100. Heine M, Groc L, Frischknecht R, Beique JC, Lounis B, Rumbaugh G, Huganir RL, Cognet L, Choquet D (2008) Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320:201–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Saxton MJ (2012) Wanted: a positive control for anomalous subdiffusion. Biophys J 103:2411–2422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Destainville N, Sauliere A, Salome L (2008) Comment to the article by Michael J Saxton: A biological interpretation of transient anomalous subdiffusion I qualitative model. Biophys J 95:3117–3119 author reply 3120-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank our colleagues at CIML and IPBS, especially Evert Haanappel for the preparation of the figures and careful reading of this manuscript. This work was supported by the Ministère de l’Enseignement Supérieur et de la Recherche (ANR-09-PIRI-0008-03, ANR-10-BLAN-1214, ANR-10-INBS-04 France BioImaging, and ANR-11-LABX-0054 Labex INFORM), Aix-Marseille Université (ANR-11-IDEX-0001-02 A*MIDEX), and Université de Toulouse and institutional funding from the Centre National de la Recherche Scientifique and the Institut National de la Santé et de la Recherche Médicale.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Didier Marguet .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Marguet, D., Salomé, L. (2018). Lateral Diffusion in Heterogeneous Cell Membranes. In: Bassereau, P., Sens, P. (eds) Physics of Biological Membranes. Springer, Cham. https://doi.org/10.1007/978-3-030-00630-3_7

Download citation

Publish with us

Policies and ethics