GPCR-Based Dopamine Sensors—A Detailed Guide to Inform Sensor Choice for In Vivo Imaging
Abstract
:1. Introduction
1.1. Measuring Neuromodulator Release During Behavior
1.2. Heterogeneity of Brain Dopamine Systems
1.3. Measuring Dopamine Across Brain Regions
1.4. Sensor Choice Depends on Brain Region Dopamine Levels and Other Experimental Modalities
2. Currently Available Methods to Measure Dopamine Release
2.1. Analytical Chemistry: Microdialysis (In Vivo) and FSCV (Ex Vivo and In Vivo)
2.2. False Fluorescent Neurotransmitters (Ex Vivo)
2.3. Carbon Nanotubes (Ex Vivo)
2.4. GPCR FRET-Based Sensors: CNiFERs (Ex Vivo and In Vivo)
2.5. GPCR Signal Transduction Sensors: iTango2 and SPARK (Ex Vivo and In Vivo)
2.6. Genetically Encoded Calcium Sensors (Ex Vivo and In Vivo)
3. Catalogue of GPCR Biosensors for Dopamine
3.1. The GPCR Dopamine Sensor Toolbox (Ex Vivo and In Vivo)
3.2. Advantages of GPCR Dopamine Biosensors
3.3. Limitations of GPCR Dopamine Biosensors
4. Regional Heterogeneity of Dopamine Systems Across the Brain
4.1. Mapping Dopamine Average Content Using Biochemistry
4.2. Mapping Basal Dopamine Levels Using In Vivo Microdialysis
4.3. Insights into Phasic Dopamine Levels Using FSCV
5. Practical Considerations for Sensor Choice: One Sensor Does Not Fit All
5.1. Matching Brain Region Dopamine Levels to Sensor Affinity and Dynamic Range
5.1.1. Affinity
5.1.2. Dynamic Range
5.1.3. Sensor Choice Based on Affinity and Dynamic Range
5.1.4. Published In vivo Validations of DA Sensors in Brain Regions with Dense vs. Sparse Innervation
5.2. Sensor Molecular Specificity Matters in Brain Regions with Dual Dopamine/Norepinephrine Innervation
5.3. Maximizing Sensor Kinetics Allows to Sparse out Individual Transients in Response to Closely Related Stimuli
5.4. Future Developments in Sensor Brightness/Subcellular Expression will Improve 1 and 2-Photon Imaging
5.5. Sensor Color Spectra Permits Dual Imaging and Multiplexing with Optogenetics and Photopharmacology
5.6. Molecular Scaffold as a Double-Edged Sword for Pharmacology and Drug Discovery
6. Piloting Sensor Use in the Laboratory
6.1. Sensor Validation at the Neuroanatomical Level
6.2. Sensor Validation In Vivo Using Optogenetic Stimulation
6.3. Sensor Validation In Vivo Using Pharmacology
6.4. Sensor Validation In Vivo Using Behavioral Stimulation
7. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
AAV | Adeno-associated virus |
Amy | Amygdala |
AP | Action potential |
Au1 | Primary auditory cortex |
BNST | Bed nucleus of the stria terminalis |
CAG | Human cytomegalovirus promoter |
cAMP | Cyclic adenosine monophosphate |
CNiFERs | Cell-based neurotransmitter fluorescent engineered reporters |
CNO | Clozapine-n-oxide |
cpFP | Circularly-permuted fluorescent protein |
cpGFP | Circularly-permuted green fluorescent protein |
cpmApple | Circularly-permuted mApple (fluorescent protein) |
CPu | Caudate-Putamen (= striatum) |
CRB | Cerebellum |
DA | Dopamine |
dFF | Normalized fluorescent response (ΔF/F) |
DR | Dorsal raphe nuclei |
DRD1-5 | Genes encoding D1-D5 dopamine receptors |
EC50 | Half maximal effective concentration |
Emis | Emission wavelength |
ENT | Enthorhinal cortex |
Exc | Excitation wavelength |
FFNs | False fluorescent neurotransmitters |
FRET | Förster resonance energy transfer |
FSCV | Fast-scan cyclic voltammetry |
GECIs | Genetically-encoded calcium indicators |
GFAP | Glial fibrillary acidic protein |
GPCR | G protein-coupled receptor |
GPe | Globus pallidus externus |
GRAB | GPCR-activation based sensors |
GTP | Guanosine triphosphate |
HEK-293 | Human embryonic kidney cell line |
HPC | Hippocampal formation |
HPLC | High-performance liquid chromatography |
hSyn | Human synapsin promoter |
Hyp | Hypothalamus |
Kd | Dissociation constant |
LS | Lateral septum |
M1 | Primary motor cortex |
M2 | Secondary motor cortex |
mPFC | Medial prefrontal cortex |
MS | Medial septum |
NAc | Nucleus accumbens |
ND | Not determined |
NE | Norepinephrine |
OT | Olfactory tubercle |
PBP | Periplasmic Binding Protein |
PVT | Paraventricular thalamus |
ROI | Region of Interest |
SN | Substantia nigra |
SNc | Subtantia nigra pars compacta |
SNR | Signal-to-noise ratio |
SWCNT | Single-walled carbon nanotubes |
TeA | Temporal association cortex |
TEV | Tobacco Etch Virus peptide sequence |
TIRF | Total internal reflection microscopy |
TRE | Tetracycline response element |
tTA | Tetracycline-controlled transactivator |
VP | Ventral pallidum |
VMAT2 | Vesicular monoamine transporter 2 |
VTA | Ventral Tegmental Area |
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Sensor | Molecular Scaffold | Affinity (Kd/EC50) | Dynamic Range (dFFmax) | Molecular Specificity vs. NE | On Kinetics: t1/2 Rise Time | Off Kinetics: t1/2 Decay Time | 1-Photon Exc/Emis | Source |
---|---|---|---|---|---|---|---|---|
dLight1.1 | DRD1 | 330 nM * | 230% * | 70-fold | 10 ms ** | 100 ms ** | 490/517 nm | [58] |
dLight1.2 | DRD1 | 765 nM * | 340% * | ND | 9.5 ms ** | 90 ms ** | 490/517 nm | [58] |
dLight1.3a | DRD1 | 2300 nM * | 660% * | ND | ND | ND | ND | [58] |
dLight1.3b | DRD1 | 1600 nM * | 930% * | 270-fold | ND | ND | ND | [58,101] |
dLight1.4 | DRD4 | 4 nM * | 170% * | ND | ND | ND | ND | [58] |
dLight1.5 | DRD2 | 110 nM * | 180% * | ND | ND | ND | ND | [58] |
RdLight1 (red) | DRD1 | 860 nM * | 250% * | 60-fold | 14 ms ** | 400 ms ** | 560/588 nm | [59] |
YdLight1 (yellow) | DRD1 | 1630 nM * | 310% * | ND | ND | ND | 514/525 nm | [59] |
GRAB-DA1m | DRD2 | 130 nM * | 90% * | 10-fold | 60 ms * | 710 ms * | 490/510 nm | [60] |
GRAB-DA1h | DRD2 | 10 nM * | 90% * | 10-fold | 140 ms * | 2520 ms * | 490/510 nm | [60] |
GRAB-DA2m | DRD2 | 90 nM * | 340% * | 22-fold | 40 ms * | 1300 ms * | ND | [61] † |
GRAB-DA2h | DRD2 | 7 nM * | 280% * | 15-fold | 50 ms * | 7300 ms * | 500/520 nm | [61] † |
GRAB-rDA1m (red-shifted) | DRD2 | 95 nM * | 150% * | 15-fold | 80 ms * | 770 ms * | 565/595 nm | [61] † |
GRAB-rDA1h (red-shifted) | DRD2 | 4 nM * | 100% * | 10-fold | 60 ms * | 2150 ms * | 565/595 nm | [61] † |
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Labouesse, M.A.; Cola, R.B.; Patriarchi, T. GPCR-Based Dopamine Sensors—A Detailed Guide to Inform Sensor Choice for In Vivo Imaging. Int. J. Mol. Sci. 2020, 21, 8048. https://doi.org/10.3390/ijms21218048
Labouesse MA, Cola RB, Patriarchi T. GPCR-Based Dopamine Sensors—A Detailed Guide to Inform Sensor Choice for In Vivo Imaging. International Journal of Molecular Sciences. 2020; 21(21):8048. https://doi.org/10.3390/ijms21218048
Chicago/Turabian StyleLabouesse, Marie A., Reto B. Cola, and Tommaso Patriarchi. 2020. "GPCR-Based Dopamine Sensors—A Detailed Guide to Inform Sensor Choice for In Vivo Imaging" International Journal of Molecular Sciences 21, no. 21: 8048. https://doi.org/10.3390/ijms21218048