Next generation genetically encoded fluorescent sensors for serotonin

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Abstract

We developed a family of genetically encoded serotonin (5-HT) sensors (sDarken) on the basis of the native 5-HT1A receptor and circularly permuted GFP. sDarken 5-HT sensors are bright in the unbound state and diminish their fluorescence upon binding of 5-HT. Sensor variants with different affinities for serotonin were engineered to increase the versatility in imaging of serotonin dynamics. Experiments in vitro and in vivo showed the feasibility of imaging serotonin dynamics with high temporal and spatial resolution. As demonstrated here, the designed sensors show excellent membrane expression, have high specificity and a superior signal-to-noise ratio, detect the endogenous release of serotonin and are suitable for two-photon in vivo imaging.

Abstract

Genetically encoded sensors have been developed and become versatile tools for imaging serotonin dynamics. Here, authors developed a family of serotonin (5-HT) sensors (sDarken), three variants with different affinities for 5-HT enable high spatiotemporal resolution of 5-HT dynamics.

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Most cited references 38

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NIH Image to ImageJ: 25 years of image analysis

Kevin W Eliceiri, Caroline A Schneider, Wayne S Rasband (2019)

For the past twenty five years the NIH family of imaging software, NIH Image and ImageJ have been pioneers as open tools for scientific image analysis. We discuss the origins, challenges and solutions of these two programs, and how their history can serve to advise and inform other software projects.

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Ultra-sensitive fluorescent proteins for imaging neuronal activity

Wen-Wen Chen, Trevor J. Wardill, Yi Sun … (2013)

Summary Fluorescent calcium sensors are widely used to image neural activity. Using structure-based mutagenesis and neuron-based screening, we developed a family of ultra-sensitive protein calcium sensors (GCaMP6) that outperformed other sensors in cultured neurons and in zebrafish, flies, and mice in vivo. In layer 2/3 pyramidal neurons of the mouse visual cortex, GCaMP6 reliably detected single action potentials in neuronal somata and orientation-tuned synaptic calcium transients in individual dendritic spines. The orientation tuning of structurally persistent spines was largely stable over timescales of weeks. Orientation tuning averaged across spine populations predicted the tuning of their parent cell. Although the somata of GABAergic neurons showed little orientation tuning, their dendrites included highly tuned dendritic segments (5 - 40 micrometers long). GCaMP6 sensors thus provide new windows into the organization and dynamics of neural circuits over multiple spatial and temporal scales.

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An optimized fluorescent probe for visualizing glutamate neurotransmission

Jonathan S. Marvin, Bart G. Borghuis, Lin Tian … (2013)

We describe an intensity-based glutamate-sensing fluorescent reporter (“iGluSnFR”) with signal-to-noise ratio and kinetics appropriate for in vivo imaging. We engineered iGluSnFR in vitro to maximize its fluorescence change, and validated its utility for visualizing glutamate release by neurons and astrocytes in increasingly intact neurological systems. In hippocampal culture, iGluSnFR detected single field stimulus-evoked glutamate release events. In pyramidal neurons in acute brain slices, glutamate uncaging at single spines showed that iGluSnFR responds robustly and specifically to glutamate in situ, and responses correlate with voltage changes. In mouse retina, iGluSnFR-expressing neurons showed intact light-evoked excitatory currents, and the sensor revealed tonic glutamate signaling in response to light stimuli. In worms, glutamate signals preceded and predicted post-synaptic calcium transients. In zebrafish, iGluSnFR revealed spatial organization of direction-selective synaptic activity in the optic tectum. Finally, in mouse forelimb motor cortex, iGluSnFR expression in layer V pyramidal neurons revealed task-dependent single-spine activity during running.

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Author and article information

Contributors

Olivia Andrea Masseck:

ORCID: http://orcid.org/0000-0002-1541-2388

masseck@uni-bremen.de

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2041-1723

Publication date (Electronic): 6 December 2022

Publication date PMC-release: 6 December 2022

Publication date Collection: 2022

Volume: 13

Electronic Location Identifier: 7525

Affiliations

[1 ]GRID grid.7704.4, ISNI 0000 0001 2297 4381, Synthetic Biology, , University of Bremen, ; Bremen, Germany

[2 ]GRID grid.424247.3, ISNI 0000 0004 0438 0426, Neuroimmunology and Imaging Group, , German Center for Neurodegenerative Diseases (DZNE), ; Bonn, Germany

[3 ]GRID grid.13648.38, ISNI 0000 0001 2180 3484, Synaptic Wiring and Information Processing, , Center for Molecular Neurobiology (ZMNH), UKE, ; Hamburg, Germany

[4 ]GRID grid.5570.7, ISNI 0000 0004 0490 981X, Cellular Neurobiology, Department of Biology and Biotechnology, , Ruhr University Bochum, ; Bochum, Germany

[5 ]GRID grid.7700.0, ISNI 0000 0001 2190 4373, Department of Neurophysiology, , University of Heidelberg, Mannheim, ; Mannheim, Germany

Author information

Monika Müller http://orcid.org/0000-0003-2995-1523

Lutz Wallhorn http://orcid.org/0000-0001-6238-7982

Mauro Pulin http://orcid.org/0000-0001-6255-0276

Tim Ziebarth http://orcid.org/0000-0001-6673-198X

Jill Gerdey http://orcid.org/0000-0002-4528-9421

J. Simon Wiegert http://orcid.org/0000-0003-0893-9349

Andreas Reiner http://orcid.org/0000-0003-0802-7278

Martin Fuhrmann http://orcid.org/0000-0001-7672-2913

Olivia Andrea Masseck http://orcid.org/0000-0002-1541-2388

Article

Publisher ID: 35200

DOI: 10.1038/s41467-022-35200-w

PMC ID: 9726753

PubMed ID: 36473867

SO-VID: cf7ada13-c347-4129-a83a-b86f28165675

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 28 February 2022

Date accepted : 22 November 2022

Funding

Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);

Award ID: 4692/6-1

Award ID: 122679504

Award ID: RE 3101/3-1

Award ID: WI4485-3/2

Award Recipient : Olivia Andrea Masseck

Funded by: FundRef https://doi.org/10.13039/100010663, EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council);

Award ID: MicroSynCom 865618

Award Recipient : Olivia Andrea Masseck

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Keywords: imaging,neuroscience

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ScienceOpen disciplines: Uncategorized

Keywords: imaging, neuroscience

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Next generation genetically encoded fluorescent sensors for serotonin

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Karger: Neurology and Neuroscience

Most cited references 38

NIH Image to ImageJ: 25 years of image analysis

Ultra-sensitive fluorescent proteins for imaging neuronal activity

An optimized fluorescent probe for visualizing glutamate neurotransmission

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