Tracking of single receptor molecule mobility in neuronal membranes: A quick theoretical and practical guide

Journal of Neuroendocrinology

Volumn 25, Issue 11, 2013, Pages 1231-1237

  Kwakowsky, A ^a   Potapov, D ^a   Abraham I M ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Fluorophores; Neurones; Receptors; Single molecule tracking; Total internal reflection fluorescence microscopy

Indexed keywords

AMPA RECEPTOR; CORTICOSTERONE; FLUORESCENT DYE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR PROTEIN; MEMBRANE PROTEIN;

BIOPHYSICS; CELL TYPE; DIFFUSION; FLUORESCENCE ANALYSIS; HUMAN; IMAGE ANALYSIS; MOLECULAR IMAGING; NERVE CELL; NERVE CELL MEMBRANE; NEUROENDOCRINOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SINGLE MOLECULE IMAGING; SYNAPSE; THEORY; ANIMAL; CELL MEMBRANE; DEVICES; PROCEDURES; ULTRASTRUCTURE;

ANIMALS; CELL MEMBRANE; MEMBRANE PROTEINS; MOLECULAR IMAGING; NEURONS;

EID: 84886670743     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12083     Document Type: Review

References (76)

1. Ritchie K, Kusumi A. Single molecule probe scanning optical force imaging microscope for viewing live cells. J Biol Phys 2002; 28: 619-626.
2. Neuman KC, Nagy A. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods 2008; 5: 491-505.
3. Yildiz A, Selvin PR. Fluorescence imaging with one nanometer accuracy: application to molecular motors. Acc Chem Res 2005; 38: 574-582.
4. Weiss S. Measuring conformational dynamics of biomolecules by single molecule fluorescence spectroscopy. Nat Struct Biol 2000; 7: 724-729.
5. Axelrod D. Total internal reflection fluorescence microscopy in cell biology. Traffic 2001; 2: 764-774.
6. Courty S, Luccardini C, Bellaiche Y, Cappello G, Dahan M. Tracking individual kinesin motors in living cells using single quantum-dot imaging. Nano Lett 2006; 6: 1491-1495.
7. Sako Y, Yanagida T. Single-molecule visualization in cell biology. Nat Rev Mol Cell Biol 2003; 9(Suppl.): SS1-SS5.
8. Giepmans BN, Deerinck TJ, Smarr BL, Jones YZ, Ellisman MH. Correlated light and electron microscopic imaging of multiple endogenous proteins using Quantum dots. Nat Methods 2005; 2: 743-749.
9. Nisman R, Dellaire G, Ren Y, Li R, Bazett-Jones DP. Application of quantum dots as probes for correlative fluorescence, conventional, and energy-filtered transmission electron microscopy. J Histochem Cytochem 2004; 52: 13-18.
10. Giepmans BN, Adams SR, Ellisman MH, Tsien RY. The fluorescent toolbox for assessing protein location and function. Science 2006; 312: 217-224.
11. Sundara Rajan S, Vu TQ. Quantum dots monitor TrkA receptor dynamics in the interior of neural PC12 cells. Nano Lett 2006; 6: 2049-2059.
12. Cui B, Wu C, Chen L, Ramirez A, Bearer EL, Li WP, Mobley WC, Chu S. One at a time, live tracking of NGF axonal transport using quantum dots. Proc Natl Acad Sci USA 2007; 104: 13666-13671.
13. Chang JC, Tomlinson ID, Warnement MR, Ustione A, Carneiro AM, Piston DW, Blakely RD, Rosenthal SJ. Single molecule analysis of serotonin transporter regulation using antagonist-conjugated quantum dots reveals restricted, p38 MAPK-dependent mobilization underlying uptake activation. J Neurosci 2012; 32: 8919-8929.
14. Bouzigues C, Dahan M. Transient directed motions of GABA(A) receptors in growth cones detected by a speed correlation index. Biophys J 2007; 92: 654-660.
15. Groc L, Choquet D, Chaouloff F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci 2008; 11: 868-870.
16. Tani T, Miyamoto Y, Fujimori KE, Taguchi T, Yanagida T, Sako Y, Harada Y. Trafficking of a ligand-receptor complex on the growth cones as an essential step for the uptake of nerve growth factor at the distal end of the axon: a single-molecule analysis. J Neurosci 2005; 25: 2181-2191.
17. Dityatev A, Seidenbecher CI, Schachner M. Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci 2010; 33: 503-512.
18. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 2009; 12: 897-904.
19. Hern JA, Baig AH, Mashanov GI, Birdsall B, Corrie JE, Lazareno S, Molloy JE, Birdsall NJ. Formation and dissociation of M1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules. Proc Natl Acad Sci USA 2010; 107: 2693-2698.
20. Kasai RS, Suzuki KG, Prossnitz ER, Koyama-Honda I, Nakada C, Fujiwara TK, Kusumi A. Full characterization of GPCR monomer-dimer dynamic equilibrium by single molecule imaging. J Cell Biol 2011; 192: 463-480.
21. Bannai H, Levi S, Schweizer C, Dahan M, Triller A. Imaging the lateral diffusion of membrane molecules with quantum dots. Nat Protoc 2006; 1: 2628-2634.
22. Michalet X, Pinaud FF, Bentolila LA, Tsay JM, Doose S, Li JJ, Sundaresan G, Wu AM, Gambhir SS, Weiss S. Quantum dots for live cells, in vivo imaging, and diagnostics. Science 2005; 307: 538-544.
23. Xia T, Li N, Fang X. Single-molecule fluorescence imaging in living cells. Annu Rev Phys Chem 2013; 644: 59-80.
24. Ha T, Tinnefeld P. Photophysics of fluorescent probes for single-molecule biophysics and super-resolution imaging. Annu Rev Phys Chem 2012; 63: 595-617.
25. Ekimov AI, Onuschenko AA. Interband absorption of light in a semiconductor sphere. Sov Phys Semicond 1982; 16: 775-778.
26. Peng ZA, Peng X. Formation of high-quality CdTe, CdSe, and CdS nanocrystals using CdO as precursor. J Am Chem Soc 2001; 123: 183-184.
27. Parak WJ, Gerion D, Zanchet D, Woerz AS, Pellegrino T, Micheel C, Williams SC, Seitz M, Bruehl RE, Bryant Z, Bustamante C, Bertozzi CR, Alivisatos AP. Conjugation of DNA to silanized colloidal semiconductor nanocrystalline quantum dots. Chem Mater 2002; 14: 2113-2119.
28. Jaiswal JK, Simon SM. Potentials and pitfalls of fluorescent quantum dots for biological imaging. Trends Cell Biol 2004; 14: 497-504.
29. Fomenko V, Nesbitt DJ. Solution control of radiative and nonradiative lifetimes: a novel contribution to quantum dot blinking suppression. Nano Lett 2008; 8: 287-293.
30. Groc L, Lafourcade M, Heine M, Renner M, Racine V, Sibarita JB, Lounis B, Choquet D, Cognet L. Surface trafficking of neurotransmitter receptor: comparison between single-molecule/quantum dot strategies. J Neurosci 2007; 27: 12433-12437.
31. Dahan M, Levi S, Luccardini C, Rostaing P, Riveau B, Triller A. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 2003; 302: 442-445.
32. Pathak S, Cao E, Davidson MC, Jin S, Silva GA. Quantum dot applications to neuroscience: new tools for probing neurons and glia. J Neurosci 2006; 26: 1893-1895.
33. Groc L, Heine M, Cognet L, Brickley K, Stephenson FA, Lounis B, Choquet D. Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat Neurosci 2004; 7: 695-696.
34. Spanhel L, Haase M, Weller H, Henglein A. Photochemistry of colloidal semiconductors.20. Surface modification and stability of strong luminescing CdS particles. J Am Chem Soc 1987; 109: 5649-5655.
35. Jaiswal JK, Goldman ER, Mattoussi H, Simon SM. Use of quantum dots for live cell imaging. Nat Methods 2004; 1: 73-78.
36. Day RN, Davidson MW. The fluorescent protein palette: tools for cellular imaging. Chem Soc Rev 2009; 38: 2887-2921.
37. Hastie P, Ulbrich MH, Wang HL, Arant RJ, Lau AG, Zhang Z, Isacoff EY, Chen L. AMPA receptor/TARP stoichiometry visualized by single-molecule subunit counting. Proc Natl Acad Sci USA 2013; 110: 5163-5168.
38. Ulbrich MH, Isacoff EY. Subunit counting in membrane-bound proteins. Nat Methods 2007; 4: 319-321.
39. Martin-Fernandez ML, Clarke DT. Single molecule fluorescence detection and tracking in mammalian cells: the state-of-the-art and future perspectives. Int J Mol Sci 2012; 13: 14742-14765.
40. Berlier JE, Rothe A, Buller G, Bradford J, Gray DR, Filanoski BJ, Telford WG, Yue S, Liu J, Cheung CY, Chang W, Hirsch JD, Beechem JM, Haugland RP, Haugland RP. Quantitative comparison of long-wavelength Alexa Fluor dyes to Cy dyes: fluorescence of the dyes and their bioconjugates. J Histochem Cytochem 2003; 51: 1699-1712.
41. Coelho M, Maghelli N, Tolic-Norrelykke IM. Single-molecule imaging in vivo: the dancing building blocks of the cell. Integr Biol (Camb) 2013; 5: 748-758.
42. Tardin C, Cognet L, Bats C, Lounis B, Choquet D. Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J 2003; 22: 4656-4665.
43. Komatsu T, Johnsson K, Okuno H, Bito H, Inoue T, Nagano T, Urano Y. Real-time measurements of protein dynamics using fluorescence activation-coupled protein labeling method. J Am Chem Soc 2011; 133: 6745-6751.
44. Vivero-Pol L, George N, Krumm H, Johnsson K, Johnsson N. Multicolor imaging of cell surface proteins. J Am Chem Soc 2005; 127: 12770-12771.
45. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH. Multicolor and electron microscopic imaging of connexin trafficking. Science 2002; 296: 503-507.
46. Crivat G, Taraska JW. Imaging proteins inside cells with fluorescent tags. Trends Biotechnol 2012; 30: 8-16.
47. Fish KN. Total internal reflection fluorescence (TIRF) microscopy. Curr Protoc Cytom 2009; John Wiley & Sons, Inc., Hoboken, New Jersey. Chapter 12. Unit 12 8.
48. Burghardt TP, Hipp AD, Ajtai K. Around-the-objective total internal reflection fluorescence microscopy. Appl Opt 2009; 48: 6120-6131.
49. Sako Y, Hiroshima M, Pack CG, Okamoto K, Hibino K, Yamamoto A. Live cell single-molecule detection in systems biology. Wiley Interdiscip Rev Syst Biol Med 2012; 4: 183-192.
50. Tokunaga M, Imamoto N, Sakata-Sogawa K. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods 2008; 5: 159-161.
51. Gell C, Berndt M, Enderlein J, Diez S. TIRF microscopy evanescent field calibration using tilted fluorescent microtubules. J Microsc 2009; 234: 38-46.
52. Denvir DJ, Coates CG. Electron multiplying CCD technology: application to ultrasensitive detection of biomolecules. P Soc Photo-Opt Ins 2002; 4626: 502-512.
53. Wells NP, Lessard GA, Phipps ME, Goodwin PM, Lidke DS. Going beyond 2D: following membrane diffusion and topography in the IgE-Fc[epsilon]RI system using 3-dimensional tracking microscopy. Proc SPIE 7185, Single Molecule Spectroscopy and Imaging II, 71850Z (February 24, 2009) 2009; doi:10.1117/12.809412.
54. Ma J, Yang W. Three-dimensional distribution of transient interactions in the nuclear pore complex obtained from single-molecule snapshots. Proc Natl Acad Sci USA 2010; 107: 7305-7310.
55. Rogers SS, Waigh TA, Zhao X, Lu JR. Precise particle tracking against a complicated background: polynomial fitting with Gaussian weight. Phys Biol 2007; 4: 220-227.
56. Ritchie K, Shan XY, Kondo J, Iwasawa K, Fujiwara T, Kusumi A. Detection of non-Brownian diffusion in the cell membrane in single molecule tracking. Biophys J 2005; 88: 2266-2277.
57. Kusumi A, Sako Y, Yamamoto M. 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; 65: 2021-2040.
58. Qian H, Sheetz MP, Elson EL. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys J 1991; 60: 910-921.
59. Saxton M. Lateral diffusion in an archipelago. Single-particle diffusion. Biophys J 1993; 64: 1766-1780.
60. Shibata SC, Hibino K, Mashimo T, Yanagida T, Sako Y. Formation of signal transduction complexes during immobile phase of NGFR movements. Biochem Biophys Res Commun 2006; 342: 316-322.
61. Simson R, Sheets ED, Jacobson K. Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis. Biophys J 1995; 69: 989-993.
62. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, Murakoshi H, Kasai RS, Kondo J, Fujiwara T. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 2005; 34: 351-378.
63. Moerner WE, Kador L. Optical detection and spectroscopy of single molecules in a solid. Phys Rev Lett 1989; 62: 2535-2538.
64. Bats C, Groc L, Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 2007; 53: 719-734.
65. Groc L, Heine M, Cousins SL, Stephenson FA, Lounis B, Cognet L, Choquet D. NMDA receptor surface mobility depends on NR2A-2B subunits. Proc Natl Acad Sci USA 2006; 103: 18769-18774.
66. Charrier C, Ehrensperger MV, Dahan M, Levi S, Triller A. Cytoskeleton regulation of glycine receptor number at synapses and diffusion in the plasma membrane. J Neurosci 2006; 26: 8502-8511.
67. Triller A, Choquet D. Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci 2005; 28: 133-139.
68. Bouzigues C, Morel M, Triller A, Dahan M. Asymmetric redistribution of GABA receptors during GABA gradient sensing by nerve growth cones analyzed by single quantum dot imaging. Proc Natl Acad Sci USA 2007; 104: 11251-11256.
69. Groc L, Choquet D. AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell Tissue Res 2006; 326: 423-438.
70. Choquet D, Triller A. The role of receptor diffusion in the organization of the postsynaptic membrane. Nat Rev Neurosci 2003; 4: 251-265.
71. Makino H, Malinow R. AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 2009; 64: 381-390.
72. Groc L, Choquet D, Stephenson FA, Verrier D, Manzoni OJ, Chavis P. NMDA receptor surface trafficking and synaptic subunit composition are developmentally regulated by the extracellular matrix protein Reelin. J Neurosci 2007; 27: 10165-10175.
73. Karst H, Berger S, Turiault M, Tronche F, Schutz G, Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci USA 2005; 102: 19204-19207.
74. Wiegert O, Joels M, Krugers H. Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus. Learn Mem 2006; 13: 110-113.
75. Groeneweg FL, Karst H, de Kloet ER, Joels M. Rapid non-genomic effects of corticosteroids and their role in the central stress response. J Endocrinol 2011; 209: 153-167.
76. Murakoshi H, Iino R, Kobayashi T, Fujiwara T, Ohshima C, Yoshimura A, Kusumi A. Single-molecule imaging analysis of Ras activation in living cells. Proc Natl Acad Sci USA 2004; 101: 7317-7322.