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PMID: 17071660 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Transient directed motions of GABA(A) receptors in growth cones detected by a speed correlation index.

Biophysical journal ·Vol. 92 ·No. 2 ·2007-01-15 ·Pages 654-60

Bouzigues C, Dahan M

Abstract

Single-molecule tracking of membrane proteins has become an important tool for investigating dynamic processes in live cells, such as cell signaling, membrane compartmentation or trafficking. The extraction of relevant parameters, such as interaction times between molecular partners or confinement-zone sizes, from the trajectories of single molecules requires appropriate statistical methods. Here we report a new tool, the speed correlation index, designed to detect transient periods of directed motion within trajectories of diffusing molecules. The ability to detect such events in a wide range of biologically relevant parameter values (speed, diffusion coefficient, and durations of the directed period) was first established on simulated data. The method was next applied to analyze the trajectories of quantum-dot-labeled GABA(A) receptors in nerve growth cones. The use of the speed correlation index revealed that the receptors had a "conveyor belt" type of motion due to temporary interactions ( approximately 4.0 s) between the receptors and the microtubules, leading to an average directed motion (velocity approximately 0.3 mum s(-1)) in the growth-cone membrane. Our observations point to the possibility of a cytoskeleton-dependent redistribution of the sensing molecules in the membrane, which could play a role in the modulation of the cell response to external signals.

MeSH Terms
Algorithms Animals Cells, Cultured Growth Cones/metabolism,ultrastructure Microscopy, Fluorescence/methods Motion Protein Transport/physiology Rats Rats, Sprague-Dawley Receptors, GABA-A/metabolism,ultrastructure
Chemicals
Receptors, GABA-A
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bouzigues Cédric
Laboratoire Kastler Brossel, Ecole Normale Supérieure, Centre National de la Recherche Scientifique UMR 8552, Paris, France.
Dahan Maxime
References (35)
35 references, click to expand
  1. Confined diffusion without fences of a g-protein-coupled receptor as revealed by single particle tracking.
    Biophys J. 2003 Jan;84(1):356-66 PMID: 12524289
  2. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking.
    Science. 2003 Oct 17;302(5644):442-5 PMID: 14564008
  3. GABA and development of the Xenopus optic projection.
    J Neurobiol. 2002 Jun 15;51(4):272-84 PMID: 12150503
  4. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein).
    J Neurosci. 2003 Apr 1;23(7):2655-64 PMID: 12684451
  5. The subcellular distribution of GABARAP and its ability to interact with NSF suggest a role for this protein in the intracellular transport of GABA(A) receptors.
    Mol Cell Neurosci. 2001 Jul;18(1):13-25 PMID: 11461150
  6. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors.
    J Neurosci. 2005 Nov 9;25(45):10469-78 PMID: 16280585
  7. Focal loss of actin bundles causes microtubule redistribution and growth cone turning.
    J Cell Biol. 2002 May 27;157(5):839-49 PMID: 12034775
  8. Direct imaging of lateral movements of AMPA receptors inside synapses.
    EMBO J. 2003 Sep 15;22(18):4656-65 PMID: 12970178
  9. Quantum dots for live cells, in vivo imaging, and diagnostics.
    Science. 2005 Jan 28;307(5709):538-44 PMID: 15681376
  10. GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton.
    Nature. 1999 Jan 7;397(6714):69-72 PMID: 9892355
  11. Structural mosaicism on the submicron scale in the plasma membrane.
    Biophys J. 1998 Jan;74(1):297-308 PMID: 9449330
  12. Single-particle tracking: applications to membrane dynamics.
    Annu Rev Biophys Biomol Struct. 1997;26:373-99 PMID: 9241424
  13. Single quantum dot tracking based on perceptual grouping using minimal paths in a spatiotemporal volume.
    IEEE Trans Image Process. 2005 Sep;14(9):1384-95 PMID: 16190473
  14. Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3378-82 PMID: 8159755
  15. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization.
    Nat Cell Biol. 2003 Jul;5(7):626-32 PMID: 12819789
  16. NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC.
    Neuron. 2004 Jun 24;42(6):897-912 PMID: 15207235
  17. Single-particle tracking: models of directed transport.
    Biophys J. 1994 Nov;67(5):2110-9 PMID: 7858148
  18. Single-molecule imaging of the H-ras membrane-anchor reveals domains in the cytoplasmic leaflet of the cell membrane.
    Biophys J. 2004 Jan;86(1 Pt 1):609-16 PMID: 14695305
  19. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems.
    Biophys J. 1991 Oct;60(4):910-21 PMID: 1742458
  20. Detection of confinement and jumps in single-molecule membrane trajectories.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2006 Jan;73(1 Pt 1):011915 PMID: 16486193
  21. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells.
    Biophys J. 1993 Nov;65(5):2021-40 PMID: 8298032
  22. Strychnine-sensitive stabilization of postsynaptic glycine receptor clusters.
    J Cell Sci. 1998 Feb;111 ( Pt 3):335-45 PMID: 9427682
  23. Cytoskeletal remodeling during growth cone-target interactions.
    J Cell Biol. 1993 Jun;121(6):1369-83 PMID: 8509456
  24. Postsynaptic scaffold proteins at non-synaptic sites. The role of postsynaptic scaffold proteins in motor-protein-receptor complexes.
    EMBO Rep. 2005 Jan;6(1):22-7 PMID: 15643447
  25. Single-molecule analysis of chemotactic signaling in Dictyostelium cells.
    Science. 2001 Oct 26;294(5543):864-7 PMID: 11679673
  26. Signaling pathway downstream of GABAA receptor in the growth cone.
    J Neurochem. 1996 Oct;67(4):1426-34 PMID: 8858924
  27. Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis.
    Biophys J. 1995 Sep;69(3):989-93 PMID: 8519998
  28. Nerve growth cone guidance mediated by G protein-coupled receptors.
    Nat Neurosci. 2002 Sep;5(9):843-8 PMID: 12161754
  29. Touch and go: guidance cues signal to the growth cone cytoskeleton.
    Curr Opin Neurobiol. 2005 Oct;15(5):521-6 PMID: 16143510
  30. Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells.
    J Cell Biol. 2002 Jul 8;158(1):31-7 PMID: 12105180
  31. GABAA receptor-associated protein traffics GABAA receptors to the plasma membrane in neurons.
    J Neurosci. 2004 Dec 15;24(50):11429-38 PMID: 15601949
  32. Fast and reversible trapping of surface glycine receptors by gephyrin.
    Nat Neurosci. 2001 Mar;4(3):253-60 PMID: 11224541
  33. Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons.
    J Neurosci. 1996 May 15;16(10):3166-77 PMID: 8627355
  34. Signaling complexes: biophysical constraints on intracellular communication.
    Annu Rev Biophys Biomol Struct. 1998;27:59-75 PMID: 9646862
  35. Relationship of lipid rafts to transient confinement zones detected by single particle tracking.
    Biophys J. 2002 Jan;82(1 Pt 1):274-84 PMID: 11751315
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2007-01-15
Epub
2006-00-27
Pages
654-60
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1751400
Subset
IM
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