DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Ion-Switchable Quantum Dot Förster Resonance Energy Transfer Rates in Ratiometric Potassium Sensors

Abstract

The tools for optically imaging cellular potassium concentrations in real-time are currently limited to a small set of molecular indicator dyes. Quantum dot-based nanosensors are more photostable and tunable than organic indicators, but previous designs have fallen short in size, sensitivity, and selectivity. In this paper, we introduce a small, sensitive, and selective nanosensor for potassium measurements. A dynamic quencher modulates the fluorescence emitted by two different quantum dot species to produce a ratiometric signal. We characterized the potassium-modulated sensor properties and investigated the photonic interactions within the sensors. The quencher’s protonation changes in response to potassium, which modulates its Förster radiative energy transfer rate and the corresponding interaction radii with each quantum dot species. Finally, the nanosensors respond to changes in potassium concentrations typical of the cellular environment and thus provide a promising tool for imaging potassium fluxes during biological events.

Authors:
 [1];  [1];  [2];  [3];  [2];  [3];  [1]
  1. Northeastern Univ., Boston, MA (United States). Dept. of Pharmaceutical Sciences
  2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Electrical Engineering
  3. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Materials Science and Engineering
Publication Date:
Research Org.:
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Northeastern Univ., Boston, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); National Academy of Sciences Ford Foundation (United States)
OSTI Identifier:
1467074
Grant/Contract Number:  
FG02-07ER46474; R01NS081641; F32EB015847; 2014-PGA084488
Resource Type:
Accepted Manuscript
Journal Name:
ACS Nano
Additional Journal Information:
Journal Volume: 10; Journal Issue: 4; Journal ID: ISSN 1936-0851
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
77 NANOSCIENCE AND NANOTECHNOLOGY; FRET; ion sensing; nanosensor; optode; quantum dot

Citation Formats

Ruckh, Timothy T., Skipwith, Christopher G., Chang, Wendi, Senko, Alexander W., Bulovic, Vladimir, Anikeeva, Polina O., and Clark, Heather A. Ion-Switchable Quantum Dot Förster Resonance Energy Transfer Rates in Ratiometric Potassium Sensors. United States: N. p., 2016. Web. doi:10.1021/acsnano.5b05396.
Ruckh, Timothy T., Skipwith, Christopher G., Chang, Wendi, Senko, Alexander W., Bulovic, Vladimir, Anikeeva, Polina O., & Clark, Heather A. Ion-Switchable Quantum Dot Förster Resonance Energy Transfer Rates in Ratiometric Potassium Sensors. United States. https://doi.org/10.1021/acsnano.5b05396
Ruckh, Timothy T., Skipwith, Christopher G., Chang, Wendi, Senko, Alexander W., Bulovic, Vladimir, Anikeeva, Polina O., and Clark, Heather A. Mon . "Ion-Switchable Quantum Dot Förster Resonance Energy Transfer Rates in Ratiometric Potassium Sensors". United States. https://doi.org/10.1021/acsnano.5b05396. https://www.osti.gov/servlets/purl/1467074.
@article{osti_1467074,
title = {Ion-Switchable Quantum Dot Förster Resonance Energy Transfer Rates in Ratiometric Potassium Sensors},
author = {Ruckh, Timothy T. and Skipwith, Christopher G. and Chang, Wendi and Senko, Alexander W. and Bulovic, Vladimir and Anikeeva, Polina O. and Clark, Heather A.},
abstractNote = {The tools for optically imaging cellular potassium concentrations in real-time are currently limited to a small set of molecular indicator dyes. Quantum dot-based nanosensors are more photostable and tunable than organic indicators, but previous designs have fallen short in size, sensitivity, and selectivity. In this paper, we introduce a small, sensitive, and selective nanosensor for potassium measurements. A dynamic quencher modulates the fluorescence emitted by two different quantum dot species to produce a ratiometric signal. We characterized the potassium-modulated sensor properties and investigated the photonic interactions within the sensors. The quencher’s protonation changes in response to potassium, which modulates its Förster radiative energy transfer rate and the corresponding interaction radii with each quantum dot species. Finally, the nanosensors respond to changes in potassium concentrations typical of the cellular environment and thus provide a promising tool for imaging potassium fluxes during biological events.},
doi = {10.1021/acsnano.5b05396},
journal = {ACS Nano},
number = 4,
volume = 10,
place = {United States},
year = {Mon Apr 18 00:00:00 EDT 2016},
month = {Mon Apr 18 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 44 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Picosecond Energy Transfer in Quantum Dot Langmuir−Blodgett Nanoassemblies
journal, December 2003

  • Achermann, Marc; Petruska, Melissa A.; Crooker, Scott A.
  • The Journal of Physical Chemistry B, Vol. 107, Issue 50
  • DOI: 10.1021/jp036497r

Spatial Distribution of Synaptically Activated Sodium Concentration Changes in Cerebellar Purkinje Neurons
journal, January 1997


Potassium ion recognition by 15-crown-5 functionalized CdSe/ZnS quantum dots in H 2 O
journal, January 2006

  • Chen, Chun-Yen; Cheng, Chiu-Ting; Lai, Chih-Wei
  • Chem. Commun., Issue 3
  • DOI: 10.1039/B512677K

Multiplexed Flow Cytometric Sensing of Blood Electrolytes in Physiological Samples Using Fluorescent Bulk Optode Microspheres
journal, November 2007

  • Xu, Chao; Wygladacz, Katarzyna; Retter, Robert
  • Analytical Chemistry, Vol. 79, Issue 24
  • DOI: 10.1021/ac7016212

Ion-Selective Optodes Measure Extracellular Potassium Flux in Excitable Cells: Ion-Selective Optodes Measure Extracellular Potassium Flux in Excitable Cells …
journal, August 2009

  • Harjes, Daniel I.; Dubach, J. Matthew; Rosenzweig, Anthony
  • Macromolecular Rapid Communications, Vol. 31, Issue 2
  • DOI: 10.1002/marc.200900297

K+-selective nanospheres: maximising response range and minimising response time
journal, January 2006

  • Ruedas-Rama, Maria Jose; Hall, Elizabeth A. H.
  • The Analyst, Vol. 131, Issue 12
  • DOI: 10.1039/b608901a

Carrier-Based Ion-Selective Electrodes and Bulk Optodes. 1. General Characteristics
journal, December 1997

  • Bakker, Eric; Bühlmann, Philippe; Pretsch, Ernö
  • Chemical Reviews, Vol. 97, Issue 8, p. 3083-3132
  • DOI: 10.1021/cr940394a

Enhancing humoral responses to a malaria antigen with nanoparticle vaccines that expand Tfh cells and promote germinal center induction
journal, January 2012

  • Moon, J. J.; Suh, H.; Li, A. V.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 4
  • DOI: 10.1073/pnas.1112648109

Long-range resonance transfer of electronic excitations in close-packed CdSe quantum-dot solids
journal, September 1996


Unconventional Role of the Inwardly Rectifying Potassium Channel Kir2.2 as a Constitutive Activator of RelA in Cancer
journal, December 2012


Biodegradable Optode-Based Nanosensors for in Vivo Monitoring
journal, June 2012

  • Balaconis, Mary K.; Clark, Heather A.
  • Analytical Chemistry, Vol. 84, Issue 13
  • DOI: 10.1021/ac301137c

Selectivity of ion-sensitive bulk optodes
journal, September 1992

  • Bakker, Eric.; Simon, Wilhelm.
  • Analytical Chemistry, Vol. 64, Issue 17
  • DOI: 10.1021/ac00041a012

Synthesis of a Sensitive and Selective Potassium-Sensing Fluoroionophore
journal, February 2010

  • Carpenter, Richard D.; Verkman, A. S.
  • Organic Letters, Vol. 12, Issue 6
  • DOI: 10.1021/ol902836c

Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging
journal, October 2012


Calcium Green FlAsH as a genetically targeted small-molecule calcium indicator
journal, June 2007

  • Tour, Oded; Adams, Stephen R.; Kerr, Rex A.
  • Nature Chemical Biology, Vol. 3, Issue 7
  • DOI: 10.1038/nchembio.2007.4

Ion-Selective Nano-optodes Incorporating Quantum Dots
journal, July 2007

  • Dubach, J. Matthew; Harjes, Daniel I.; Clark, Heather A.
  • Journal of the American Chemical Society, Vol. 129, Issue 27
  • DOI: 10.1021/ja072522l

Multiplexed Sensing of Ions with Barcoded Polyelectrolyte Capsules
journal, November 2011

  • del Mercato, Loretta L.; Abbasi, Azhar Z.; Ochs, Markus
  • ACS Nano, Vol. 5, Issue 12
  • DOI: 10.1021/nn203344w

Therapeutic cell engineering with surface-conjugated synthetic nanoparticles
journal, August 2010

  • Stephan, Matthias T.; Moon, James J.; Um, Soong Ho
  • Nature Medicine, Vol. 16, Issue 9
  • DOI: 10.1038/nm.2198

Localizable and Highly Sensitive Calcium Indicator Based on a BODIPY Fluorophore
journal, June 2010

  • Kamiya, Mako; Johnsson, Kai
  • Analytical Chemistry, Vol. 82, Issue 15
  • DOI: 10.1021/ac100741t

K+ waves in brain cortex visualized using a long-wavelength K+-sensing fluorescent indicator
journal, October 2005

  • Padmawar, Prashant; Yao, Xiaoming; Bloch, Orin
  • Nature Methods, Vol. 2, Issue 11
  • DOI: 10.1038/nmeth801

Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish
journal, March 2011

  • Muto, A.; Ohkura, M.; Kotani, T.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
  • DOI: 10.1073/pnas.1000887108

A Highly Potassium-Selective Ratiometric Fluorescent Indicator Based on BODIPY Azacrown Ether Excitable with Visible Light
journal, September 2005

  • Baruah, Mukulesh; Qin, Wenwu; Vallée, Renaud A. L.
  • Organic Letters, Vol. 7, Issue 20
  • DOI: 10.1021/ol051603o

Sodium Imaging of Climbing Fiber Innervation Fields in Developing Mouse Purkinje Cells
journal, May 2003

  • Scelfo, Bibiana; Strata, Piergiorgio; Knöpfel, Thomas
  • Journal of Neurophysiology, Vol. 89, Issue 5
  • DOI: 10.1152/jn.00884.2002

Two-Photon Sodium Imaging in Dendritic Spines
journal, November 2012


Sodium‐Ion‐Selective Two‐Photon Fluorescent Probe for In Vivo Imaging
journal, January 2010

  • Kim, Mi Kyung; Lim, Chang Su; Hong, Jong Tae
  • Angewandte Chemie International Edition, Vol. 49, Issue 2
  • DOI: 10.1002/anie.200904835

Sodium Sensing in Neurons with a Dendrimer-Based Nanoprobe
journal, January 2012

  • Lamy, Christophe M.; Sallin, Olivier; Loussert, Céline
  • ACS Nano, Vol. 6, Issue 2
  • DOI: 10.1021/nn203822t

Optimized ratiometric calcium sensors for functional in vivo imaging of neurons and T lymphocytes
journal, January 2014

  • Thestrup, Thomas; Litzlbauer, Julia; Bartholomäus, Ingo
  • Nature Methods, Vol. 11, Issue 2
  • DOI: 10.1038/nmeth.2773

Optical Nanosensors for Chemical Analysis inside Single Living Cells. 2. Sensors for pH and Calcium and the Intracellular Application of PEBBLE Sensors
journal, November 1999

  • Clark, Heather A.; Kopelman, Raoul; Tjalkens, Ron
  • Analytical Chemistry, Vol. 71, Issue 21
  • DOI: 10.1021/ac990630n

Fluorescent Recognition of Potassium and Calcium Ions Using Functionalised CdSe / ZnS Quantum Dots
journal, March 2009


A genetically encoded calcium indicator for chronic in vivo two-photon imaging
journal, August 2008

  • Mank, Marco; Santos, Alexandre Ferrão; Direnberger, Stephan
  • Nature Methods, Vol. 5, Issue 9, p. 805-811
  • DOI: 10.1038/nmeth.1243

Fiji: an open-source platform for biological-image analysis
journal, June 2012

  • Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2019

Multicolor Quantum Dot Encoding for Polymeric Particle-Based Optical Ion Sensors
journal, May 2007

  • Xu, Chao; Bakker, Eric
  • Analytical Chemistry, Vol. 79, Issue 10
  • DOI: 10.1021/ac0701233

Visualizing sodium dynamics in isolated cardiomyocytes using fluorescent nanosensors
journal, September 2009

  • Dubach, J. M.; Das, S.; Rosenzweig, A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
  • DOI: 10.1073/pnas.0905909106

Two-Dimensional Förster Resonant Energy Transfer in a Mixed Quantum Dot Monolayer: Experiment and Theory
journal, February 2009

  • Lunz, Manuela; Bradley, A. Louise; Chen, Wei-Yu
  • The Journal of Physical Chemistry C, Vol. 113, Issue 8
  • DOI: 10.1021/jp8087034

A Novel Optical Intracellular Imaging Approach for Potassium Dynamics in Astrocytes
journal, October 2014


Dynamic reciprocity of sodium and potassium channel expression in a macromolecular complex controls cardiac excitability and arrhythmia
journal, April 2012

  • Milstein, M. L.; Musa, H.; Balbuena, D. P.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 31
  • DOI: 10.1073/pnas.1109370109

Theoretical aspects of bulk optode membranes
journal, August 1992


Optical Nanosensors for Chemical Analysis inside Single Living Cells. 1. Fabrication, Characterization, and Methods for Intracellular Delivery of PEBBLE Sensors
journal, November 1999

  • Clark, Heather A.; Hoyer, Marion; Philbert, Martin A.
  • Analytical Chemistry, Vol. 71, Issue 21
  • DOI: 10.1021/ac990629o

Polymer-Free Optode Nanosensors for Dynamic, Reversible and Ratiometric Sodium Imaging in the Physiological Range
journal, November 2013

  • Ruckh, Timothy T.; Mehta, Ankeeta A.; Dubach, J. Matthew
  • Scientific Reports, Vol. 3, Issue 1
  • DOI: 10.1038/srep03366

Carrier-Based Ion-Selective Electrodes and Bulk Optodes. 2. Ionophores for Potentiometric and Optical Sensors
journal, June 1998

  • Bühlmann, Philippe; Pretsch, Ernö; Bakker, Eric
  • Chemical Reviews, Vol. 98, Issue 4
  • DOI: 10.1021/cr970113+

Potassium channel activation inhibits proliferation of breast cancer cells by activating a senescence program
journal, June 2013


Fluorescent indicators for cytosolic sodium
journal, November 1989


Works referencing / citing this record:

An ionophore-based persistent luminescent ‘Glow Sensor’ for sodium detection
journal, January 2019

  • Ferris, Mark S.; Behr, Madeline R.; Cash, Kevin J.
  • RSC Advances, Vol. 9, Issue 56
  • DOI: 10.1039/c9ra05313a

Rhodamine based NIR and ratiometric fluorescent sensor for selective identification of potassium ion: application in biological sample
journal, October 2018


Multifunctional fluorescent naphthalimide self-assembly system for the detection of Cu 2+ and K + and continuous sensing of organic amines and gaseous acids
journal, January 2019

  • Cao, Xinhua; Li, Yiran; Gao, Aiping
  • Journal of Materials Chemistry C, Vol. 7, Issue 34
  • DOI: 10.1039/c9tc03243f

Ratiometric optical nanoprobes enable accurate molecular detection and imaging
journal, January 2018

  • Huang, Xiaolin; Song, Jibin; Yung, Bryant C.
  • Chemical Society Reviews, Vol. 47, Issue 8
  • DOI: 10.1039/c7cs00612h