Labeling of neuronal receptors and transporters with quantum dots

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 4, Issue 6, 2012, Pages 605-619

  Chang, Jerry C ^a   Kovtun, Oleg ^a   Blakely, Randy D ^a,b   Rosenthal, Sandra J ^a,c,d  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFUNCTIONALIZATION; BIOLOGICAL RESEARCH; FLUORESCENCE IMAGING; FLUORESCENT PROBES; LIVING CELL; MEMBRANE PROTEINS; MOLECULAR ASPECTS; PHARMACOLOGICAL RESEARCH; PHOTOPHYSICAL PROPERTIES; PROTEIN TARGETS; SYNTHETIC ROUTES;

BIOLOGICAL MEMBRANES; SEMICONDUCTOR QUANTUM DOTS; SURFACE CHEMISTRY;

NEURONS;

FLUORESCENT DYE; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; QUANTUM DOT;

FLUORESCENCE IMAGING; NANOCHEMISTRY; NERVE CELL NETWORK; NERVE MEMBRANE; NEUROBIOLOGY; NEUROSCIENCE; PRIORITY JOURNAL; QUANTUM CHEMISTRY; REVIEW; SURFACE PROPERTY; SYNAPTIC TRANSMISSION;

ANIMALS; FLUORESCENT DYES; HUMANS; MOLECULAR IMAGING; MOLECULAR PROBES; NEURONS; NEUROTRANSMITTER TRANSPORT PROTEINS; PROTEIN TRANSPORT; QUANTUM DOTS; RECEPTORS, NEUROTRANSMITTER;

EID: 84867728468     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1186     Document Type: Review

References (82)

1. Rozental R, Giaume C, Spray DC. Gap junctions in the nervous system. Brain Res Rev 2000, 32:11-15.
2. Collingridge GL, Isaac JT, Wang YT. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 2004, 5:952-962.
3. Blakely RD, Defelice LJ, Galli A. Biogenic amine neurotransmitter transporters: just when you thought you knew them. Physiology 2005, 20:225-231.
4. Tsien RY. The green fluorescent protein. Annu Rev Biochem 1998, 67:509-544.
5. Bastiaens PIH, Pepperkok R. Observing proteins in their natural habitat: the living cell. Trends Biochem Sci 2000, 25:631-637.
6. Marks KM, Nolan GP. Chemical labeling strategies for cell biology. Nat Methods 2006, 3:591-596.
7. Rosenthal SJ, McBride J, Pennycook SJ, Feldman LC. Synthesis, surface studies, composition and structural characterization of CdSe, core/shell and biologically active nanocrystals. Surf Sci Rep 2007, 62:111-157.
8. Chan WC, Nie S. Quantum dot bioconjugates for ultrasensitive nonisotopic detection. Science 1998, 281:2016-2018.
9. Bruchez M, Moronne M, Gin P, Weiss S, Alivisatos AP. Semiconductor nanocrystals as fluorescent biological labels. Science 1998, 281:2013-2016.
10. Akerman ME, Chan WC, Laakkonen P, Bhatia SN, Ruoslahti E. Nanocrystal targeting in vivo. Proc Natl Acad Sci USA 2002, 99:12617-12621.
11. Gao XH, Cui YY, Levenson RM, Chung LWK, Nie SM. In vivo cancer targeting and imaging with semiconductor quantum dots. Nat Biotechnol 2004, 22:969-976.
12. Kim S, Lim YT, Soltesz EG, De Grand AM, Lee J, Nakayama A, Parker JA, Mihaljevic T, Laurence RG, Dor DM, et al. Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping. Nat Biotechnol 2004, 22:93-97.
13. 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.
14. Rosenthal SJ, Chang JC, Kovtun O, McBride JR, Tomlinson ID. Biocompatible quantum dots for biological applications. Chem Biol 2011, 18:10-24.
15. Yu WW, Qu LH, Guo WZ, Peng XG. Experimental determination of the extinction coefficient of CdTe, CdSe, and CdS nanocrystals. Chem Mater 2003, 15:2854-2860.
16. Dabbousi BO, RodriguezViejo J, Mikulec FV, Heine JR, Mattoussi H, Ober R, Jensen KF, Bawendi MG. (CdSe)ZnS core-shell quantum dots: Synthesis and characterization of a size series of highly luminescent nanocrystallites. J Phys Chem B 1997, 101:9463-9475.
17. Murray CB, Norris DJ, Bawendi MG. Synthesis and characterization of nearly monodisperse CdE (E = sulfur, selenium, tellurium) semiconductor nanocrystallites. J Am Chem Soc 1993, 115:8706-8715.
18. Talapin DV, Rogach AL, Kornowski A, Haase M, Weller H. Highly luminescent monodisperse CdSe and CdSe/ZnS nanocrystals synthesized in a hexadecylamine-trioctylphosphine oxide-trioctylphospine mixture. Nano Lett 2001, 1:207-211.
19. Bharali DJ, Lucey DW, Jayakumar H, Pudavar HE, Prasad PN. Folate-receptor-mediated delivery of InP quantum dots for bioimaging using confocal and two-photon microscopy. J Am Chem Soc 2005, 127:11364-11371.
20. Kovtun O, Tomlinson ID, Sakrikar DS, Chang JC, Blakely RD, Rosenthal SJ. Visualization of the cocaine-sensitive dopamine transporter with ligand-conjugated quantum dots. ACS Chem Neurosci 2011, 2:370-378.
21. Kucur E, Boldt FM, Cavaliere-Jaricot S, Ziegler J, Nann T. Quantitative analysis of cadmium selenide nanocrystal concentration by comparative techniques. Anal Chem 2007, 79:8987-8993.
22. Chan WCW, Maxwell DJ, Gao XH, Bailey RE, Han MY, Nie SM. Luminescent quantum dots for multiplexed biological detection and imaging. Curr Opin Biotechnol 2002, 13:40-46.
23. Jaiswal JK, Mattoussi H, Mauro JM, Simon SM. Long-term multiple color imaging of live cells using quantum dot bioconjugates. Nat Biotechnol 2003, 21:47-51.
24. Stroh M, Zimmer JP, Duda DG, Levchenko TS, Cohen KS, Brown EB, Scadden DT, Torchilin VP, Bawendi MG, Fukumura D, et al. Quantum dots spectrally distinguish multiple species within the tumor milieu in vivo. Nat Med 2005, 11:678-682.
25. Chattopadhyay PK, Price DA, Harper TF, Betts MR, Yu J, Gostick E, Perfetto SP, Goepfert P, Koup RA, De Rosa SC, et al. Quantum dot semiconductor nanocrystals for immunophenotyping by polychromatic flow cytometry. Nat Med 2006, 12:972-977.
26. Veenstra-VanderWeele J, Muller CL, Iwamoto H, Sauer JE, Owens WA, Shah CR, Cohen J, Mannangatti P, Jessen T, Thompson BJ, et al. Autism gene variant causes hyperserotonemia, serotonin receptor hypersensitivity, social impairment and repetitive behavior. Proc Natl Acad Sci USA 2012, 109:5469-5474.
27. Resch-Genger U, Grabolle M, Cavaliere-Jaricot S, Nitschke R, Nann T. Quantum dots versus organic dyes as fluorescent labels. Nat Methods 2008, 5:763-775.
28. Nirmal M, Dabbousi BO, Bawendi MG, Macklin JJ, Trautman JK, Harris TD, Brus LE. Fluorescence intermittency in single cadmium selenide nanocrystals. Nature 1996, 383:802-804.
29. Frantsuzov PA, Volkan-Kacso S, Janko B. Model of fluorescence intermittency of single colloidal semiconductor quantum dots using multiple recombination centers. Phys Rev Lett 2009, 103:207402.
30. Mahler B, Spinicelli P, Buil S, Quelin X, Hermier JP, Dubertret B. Towards non-blinking colloidal quantum dots. Nat Mater 2008, 7:659-664.
31. Wang X, Ren X, Kahen K, Hahn MA, Rajeswaran M, Maccagnano-Zacher S, Silcox J, Cragg GE, Efros AL, Krauss TD. Non-blinking semiconductor nanocrystals. Nature 2009, 459:686-689.
32. Yao J, Larson DR, Vishwasrao HD, Zipfel WR, Webb WW. Blinking and nonradiant dark fraction of water-soluble quantum dots in aqueous solution. Proc Natl Acad Sci USA 2005, 102:14284-14289.
33. Medintz IL, Uyeda HT, Goldman ER, Mattoussi H. Quantum dot bioconjugates for imaging, labelling and sensing. Nat Mater 2005, 4:435-446.
34. Wu XY, Liu HJ, Liu JQ, Haley KN, Treadway JA, Larson JP, Ge NF, Peale F, Bruchez MP. Immunofluorescent labeling of cancer marker Her2 and other cellular targets with semiconductor quantum dots. Nat Biotechnol 2003, 21:41-46.
35. Pellegrino T, Manna L, Kudera S, Liedl T, Koktysh D, Rogach AL, Keller S, Radler J, Natile G, Parak WJ. Hydrophobic nanocrystals coated with an amphiphilic polymer shell: A general route to water soluble nanocrystals. Nano Lett 2004, 4:703-707.
36. Ow H, Larson DR, Srivastava M, Baird BA, Webb WW, Wiesner U. Bright and stable core-shell fluorescent silica nanoparticles. Nano Lett 2005, 5:113-117.
37. Selvan ST, Tan TT, Ying JY. Robust, non-cytotoxic, silica-coated CdSe quantum dots with efficient photoluminescence. Adv Mater 2005, 17:1620-1625.
38. Nann T, Mulvaney P. Single quantum dots in spherical silica particles. Angew Chem, Int Ed 2004, 43: 5393-5396.
39. Mattoussi H, Mauro JM, Goldman ER, Anderson GP, Sundar VC, Mikulec FV, Bawendi MG. Self-assembly of CdSe-ZnS quantum dot bioconjugates using an engineered recombinant protein. J Am Chem Soc 2000, 122: 12142-12150.
40. Kim S, Bawendi MG. Oligomeric ligands for luminescent and stable nanocrystal quantum dots. J Am Chem Soc 2003, 125:14652-14653.
41. Pathak S, Davidson MC, Silva GA. Characterization of the functional binding properties of antibody conjugated quantum dots. Nano Lett 2007, 7:1839-1845.
42. Rosenthal SJ, Tomlinson I, Adkins EM, Schroeter S, Adams S, Swafford L, McBride J, Wang Y, DeFelice LJ, Blakely RD. Targeting cell surface receptors with ligand-conjugated nanocrystals. J Am Chem Soc 2002, 124: 4586-4594.
43. Goldman ER, Balighian ED, Mattoussi H, Kuno MK, Mauro JM, Tran PT, Anderson GP. Avidin: a natural bridge for quantum dot-antibody conjugates. J Am Chem Soc 2002, 124:6378-6382.
44. Wilchek M, Bayer EA. Introduction to avidin-biotin technology. Method Enzymol 1990, 184:5-13.
45. Chaiet L, Wolf FJ. The properties of streptavidin, a biotin-binding protein produced by Streptomycetes. Arch Biochem Biophys 1964, 106:1-5.
46. Weber PC, Ohlendorf DH, Wendoloski JJ, Salemme FR. Structural origins of high-affinity biotin binding to streptavidin. Science 1989, 243:85-88.
47. Orndorff RL, Warnement MR, Mason JN, Blakely RD, Rosenthal SJ. Quantum dot ex vivo labeling of neuromuscular synapses. Nano Lett 2008, 8:780-785.
48. Chang JC, Tomlinson ID, Warnement MR, Iwamoto H, DeFelice LJ, Blakely RD, Rosenthal SJ. A fluorescence displacement assay for antidepressant drug discovery based on ligand-conjugated quantum dots. J Am Chem Soc 2011, 133:17528-17531.
49. Jaiswal JK, Simon SM. Potentials and pitfalls of fluorescent quantum dots for biological imaging. Trends Cell Biol 2004, 14:497-504.
50. Howarth M, Chinnapen DJ, Gerrow K, Dorrestein PC, Grandy MR, Kelleher NL, El-Husseini A, Ting AY. A monovalent streptavidin with a single femtomolar biotin binding site. Nat Methods 2006, 3:267-273.
51. Howarth M, Liu W, Puthenveetil S, Zheng Y, Marshall LF, Schmidt MM, Wittrup KD, Bawendi MG, Ting AY. Monovalent, reduced-size quantum dots for imaging receptors on living cells. Nat Methods 2008, 5: 397-399.
52. Chang JC, Tomlinson ID, Warnement MR, Ustione A, Carneiro AMD, 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.
53. Kovtun O, Ross EJ, Tomlinson ID, Rosenthal SJ. A flow cytometry-based dopamine transporter binding assay using antagonist-conjugated quantum dots. Chem Commun 2012.
54. Gussin HA, Tomlinson ID, Little DM, Warnement MR, Qian HH, Rosenthal SJ, Pepperberg DR. Binding of muscimol-conjugated quantum dots to GABA(c) receptors. J Am Chem Soc 2006, 128:15701-15713.
55. Muir J, Arancibia-Carcamo IL, MacAskill AF, Smith KR, Griffin LD, Kittler JT. NMDA receptors regulate GABAA receptor lateral mobility and clustering at inhibitory synapses through serine 327 on the γ2 subunit. Proc Natl Acad Sci USA 2010, 107:16679-16684.
56. 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.
57. Levi S, Schweizer C, Bannai H, Pascual O, Charrier C, Triller A. Homeostatic regulation of synaptic GlyR numbers driven by lateral diffusion. Neuron 2008, 59: 261-273.
58. Yeow EKL, Clayton AHA. Enumeration of oligomerization states of membrane proteins in living cells by homo-FRET spectroscopy and microscopy: Theory and application. Biophys J 2007, 92:3098-3104.
59. 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.
60. Sundara Rajan S, Vu TQ. Quantum dots monitor TrkA receptor dynamics in the interior of neural PC12 cells. Nano Lett 2006, 6:2049-2059.
61. Rajan SS, Liu HY, Vu TQ. Ligand-bound quantum dot probes for studying the molecular scale dynamics of receptor endocytic trafficking in live cells. ACS Nano 2008, 2:1153-1166.
62. Fichter KM, Flajolet M, Greengard P, Vu TQ. Kinetics of G-protein-coupled receptor endosomal trafficking pathways revealed by single quantum dots. Proc Natl Acad Sci USA 2010, 107:18658-18663.
63. Charrier C, Machado P, Tweedie-Cullen RY, Rutishauser D, Mansuy IM, Triller A. A crosstalk between b1 and b3 integrins controls glycine receptor and gephyrin trafficking at synapses. Nat Neurosci 2010, 13:1388-1395.
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. Howarth M, Takao K, Hayashi Y, Ting AY. Targeting quantum dots to surface proteins in living cells with biotin ligase. Proc Natl Acad Sci USA 2005, 102: 7583-7588.
66. Mikasova L, Groc L, Choquet D, Manzoni OJ. Altered surface trafficking of presynaptic cannabinoid type 1 receptor in and out synaptic terminals parallels receptor desensitization. Proc Natl Acad Sci USA 2008, 105:18596-18601.
67. Michaluk P, Mikasova L, Groc L, Frischknecht R, Choquet D, Kaczmarek L. Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin b1 signaling. J Neurosci 2009, 29:6007-6012.
68. Renner M, Lacor PN, Velasco PT, Xu J, Contractor A, Klein WL, Triller A. Deleterious effects of amyloid β oligomers acting as an extracellular scaffold for mGluR5. Neuron 2010, 66:739-754.
69. Fernandes CC, Berg DK, Gomez-Varela D. Lateral mobility of nicotinic acetylcholine receptors on neurons is determined by receptor composition, local domain, and cell type. J Neurosci 2010, 30:8841-8851.
70. Tomlinson ID, Mason JN, Blakely RD, Rosenthal SJ. Peptide-conjugated quantum dots: imaging the angiotensin type 1 receptor in living cells. Methods Mol Biol 2005, 303:51-60.
71. Mercer AJ, Chen M, Thoreson WB. Lateral mobility of presynaptic L-type calcium channels at photoreceptor ribbon synapses. J Neurosci 2011, 31:4397-4406.
72. Jiang S, Liu AP, Duan HW, Soo J, Chen P. Labeling and tracking P2 purinergic receptors in living cells using ATP-conjugated quantum dots. Adv Funct Mater 2011, 21:2776-2780.
73. Clarke SJ, Hollmann CA, Zhang Z, Suffern D, Bradforth SE, Dimitrijevic NM, Minarik WG, Nadeau JL. Photophysics of dopamine-modified quantum dots and effects on biological systems. Nat Mater 2006, 5: 409-417.
74. Bentzen EL, Tomlinson ID, Mason J, Gresch P, Warnement MR, Wright D, Sanders-Bush E, Blakely R, Rosenthal SJ. Surface modification to reduce nonspecific binding of quantum dots in live cell assays. Bioconjug Chem 2005, 16:1488-1494.
75. C receptor binding of quantum-dot conjugates of variable ligand valency. Bioconjug Chem 2010, 21:1455-1464.
76. 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.
77. AR diffusion dynamics. Neuron 2009, 62:670-682.
78. Chen I, Howarth M, Lin W, Ting AY. Site-specific labeling of cell surface proteins with biophysical probes using biotin ligase. Nat Methods 2005, 2:99-104.
79. Cui B, Wu C, Chen L, Ramirez A, Bearer EL, Li W-P, 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.
80. Ehrensperger M-V, Hanus C, Vannier C, Triller A, Dahan M. Multiple association states between glycine receptors and gephyrin identified by SPT analysis. Biophys J 2007, 92:3706-3718.
81. Pinaud F, Clarke S, Sittner A, Dahan M. Probing cellular events, one quantum dot at a time. Nat Methods 2010, 7:275-285.
82. Chang Y-P, Pinaud F, Antelman J, Weiss S. Tracking bio-molecules in live cells using quantum dots. J Biophotonics 2008, 1:287-298.