Genetically encoded sensors for measuring histamine release both in vitro and in vivo

Hui Dong; Mengyao Li; Yuqi Yan; Tongrui Qian; Yunzhi Lin; Xiaoyuan Ma; Henry F. Vischer; Can Liu; Guochuan Li; Huan Wang; Rob Leurs; Yulong Li

doi:10.1016/j.neuron.2023.02.024

Genetically encoded sensors for measuring histamine release both in vitro and in vivo

Hui Dong, Mengyao Li, Yuqi Yan, Tongrui Qian, Yunzhi Lin, Xiaoyuan Ma, Henry F. Vischer, Can Liu, Guochuan Li, Huan Wang, Rob Leurs, Yulong Li^*

^*Corresponding author for this work

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Abstract

Histamine (HA) is a key biogenic monoamine involved in a wide range of physiological and pathological processes in both the central and peripheral nervous systems. Because the ability to directly measure extracellular HA in real time will provide important insights into the functional role of HA in complex circuits under a variety of conditions, we developed a series of genetically encoded G-protein-coupled receptor-activation-based (GRAB) HA (GRAB_HA) sensors with good photostability, sub-second kinetics, nanomolar affinity, and high specificity. Using these GRAB_HA sensors, we measured electrical-stimulation-evoked HA release in acute brain slices with high spatiotemporal resolution. Moreover, we recorded HA release in the preoptic area of the hypothalamus and prefrontal cortex during the sleep-wake cycle in freely moving mice, finding distinct patterns of HA dynamics between these specific brain regions. Thus, GRAB_HA sensors are robust tools for measuring extracellular HA transmission in both physiological and pathological processes.

Original language	English
Pages (from-to)	1564-1576.e6
Number of pages	20
Journal	Neuron
Volume	111
Issue number	10
Early online date	15 Mar 2023
DOIs	https://doi.org/10.1016/j.neuron.2023.02.024
Publication status	Published - 17 May 2023

Bibliographical note

Funding Information:
This research was supported by grants to Y.L. from the National Natural Science Foundation of China (31925017), the National Key R&D Program of China ( 2019YFE011781 ), the NIH BRAIN Initiative ( 1U01NS113358 and 1U01NS120824 ), the Beijing Municipal Science & Technology Commission ( Z220009 ), the Feng Foundation of Biomedical Research , the Clement and Xinxin Foundation , the Peking-Tsinghua Center for Life Sciences , and the State Key Laboratory of Membrane Biology at School of Life Sciences , Peking University . We thank Dr. Yi Rao for sharing the two-photon microscope and Dr. Xiaoguang Lei at PKU-CLS and the National Center for Protein Sciences at Peking University for providing support for the Opera Phenix high-content screening system and imaging platform. We thank Dr. Xiangdong Yang at Fudan University, who kindly provided HDC KO mice. Some graphics were generated using BioRender.com .

Funding Information:
This research was supported by grants to Y.L. from the National Natural Science Foundation of China (31925017), the National Key R&D Program of China (2019YFE011781), the NIH BRAIN Initiative (1U01NS113358 and 1U01NS120824), the Beijing Municipal Science & Technology Commission (Z220009), the Feng Foundation of Biomedical Research, the Clement and Xinxin Foundation, the Peking-Tsinghua Center for Life Sciences, and the State Key Laboratory of Membrane Biology at School of Life Sciences, Peking University. We thank Dr. Yi Rao for sharing the two-photon microscope and Dr. Xiaoguang Lei at PKU-CLS and the National Center for Protein Sciences at Peking University for providing support for the Opera Phenix high-content screening system and imaging platform. We thank Dr. Xiangdong Yang at Fudan University, who kindly provided HDC KO mice. Some graphics were generated using BioRender.com. Y.L. conceived and supervised the project. M.L. performed the experiments related to developing, optimizing, and characterizing the sensor in cultured HEK293T cells and neurons. Y.Y. characterized HA sensors in HEK293T cells and neurons. X.M. and H.F.V. performed the binding studies. T.Q. and M.L. performed the experiments in brain slices. H.D. Y.L. and C.L. performed the in vivo recording in freely behaving mice. G.L. and H.W. performed the characterization of the wavelength spectra of HA sensors in HEK293T cells. All authors contributed to data interpretation and analysis. Y.L. H.D. and Y.Y. wrote the manuscript with input from all other authors. Y.L. has filed patent applications, the value of which might be affected by this publication. We support inclusive, diverse, and equitable conduct of research.

Publisher Copyright:
© 2023 Elsevier Inc.

Funding

This research was supported by grants to Y.L. from the National Natural Science Foundation of China (31925017), the National Key R&D Program of China ( 2019YFE011781 ), the NIH BRAIN Initiative ( 1U01NS113358 and 1U01NS120824 ), the Beijing Municipal Science & Technology Commission ( Z220009 ), the Feng Foundation of Biomedical Research , the Clement and Xinxin Foundation , the Peking-Tsinghua Center for Life Sciences , and the State Key Laboratory of Membrane Biology at School of Life Sciences , Peking University . We thank Dr. Yi Rao for sharing the two-photon microscope and Dr. Xiaoguang Lei at PKU-CLS and the National Center for Protein Sciences at Peking University for providing support for the Opera Phenix high-content screening system and imaging platform. We thank Dr. Xiangdong Yang at Fudan University, who kindly provided HDC KO mice. Some graphics were generated using BioRender.com . This research was supported by grants to Y.L. from the National Natural Science Foundation of China (31925017), the National Key R&D Program of China (2019YFE011781), the NIH BRAIN Initiative (1U01NS113358 and 1U01NS120824), the Beijing Municipal Science & Technology Commission (Z220009), the Feng Foundation of Biomedical Research, the Clement and Xinxin Foundation, the Peking-Tsinghua Center for Life Sciences, and the State Key Laboratory of Membrane Biology at School of Life Sciences, Peking University. We thank Dr. Yi Rao for sharing the two-photon microscope and Dr. Xiaoguang Lei at PKU-CLS and the National Center for Protein Sciences at Peking University for providing support for the Opera Phenix high-content screening system and imaging platform. We thank Dr. Xiangdong Yang at Fudan University, who kindly provided HDC KO mice. Some graphics were generated using BioRender.com. Y.L. conceived and supervised the project. M.L. performed the experiments related to developing, optimizing, and characterizing the sensor in cultured HEK293T cells and neurons. Y.Y. characterized HA sensors in HEK293T cells and neurons. X.M. and H.F.V. performed the binding studies. T.Q. and M.L. performed the experiments in brain slices. H.D. Y.L. and C.L. performed the in vivo recording in freely behaving mice. G.L. and H.W. performed the characterization of the wavelength spectra of HA sensors in HEK293T cells. All authors contributed to data interpretation and analysis. Y.L. H.D. and Y.Y. wrote the manuscript with input from all other authors. Y.L. has filed patent applications, the value of which might be affected by this publication. We support inclusive, diverse, and equitable conduct of research.

Funders	Funder number
Clement and Xinxin Foundation
Feng Foundation of Biomedical Research
Peking-Tsinghua Center for Life Sciences
State Key Laboratory of Membrane Biology at School of Life Sciences , Peking University
State Key Laboratory of Membrane Biology at School of Life Sciences, Peking University
National Institutes of Health	1U01NS120824, 1U01NS113358
National Institutes of Health
National Natural Science Foundation of China	31925017
National Natural Science Foundation of China
Fudan University
Beijing Municipal Science and Technology Commission	Z220009
Beijing Municipal Science and Technology Commission
National Key Research and Development Program of China	2019YFE011781
National Key Research and Development Program of China

Keywords

genetically encoded sensor
GRAB sensor
histamine
sleep-wake cycle

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10.1016/j.neuron.2023.02.024

Genetically encoded sensors for measuring histamine release both in vitro and in vivoFinal published version, 42.7 MBLicence: Article 25fa Dutch Copyright Act

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@article{99ca4ce9d4c249f5b6b3e53e6b04c052,

title = "Genetically encoded sensors for measuring histamine release both in vitro and in vivo",

abstract = "Histamine (HA) is a key biogenic monoamine involved in a wide range of physiological and pathological processes in both the central and peripheral nervous systems. Because the ability to directly measure extracellular HA in real time will provide important insights into the functional role of HA in complex circuits under a variety of conditions, we developed a series of genetically encoded G-protein-coupled receptor-activation-based (GRAB) HA (GRABHA) sensors with good photostability, sub-second kinetics, nanomolar affinity, and high specificity. Using these GRABHA sensors, we measured electrical-stimulation-evoked HA release in acute brain slices with high spatiotemporal resolution. Moreover, we recorded HA release in the preoptic area of the hypothalamus and prefrontal cortex during the sleep-wake cycle in freely moving mice, finding distinct patterns of HA dynamics between these specific brain regions. Thus, GRABHA sensors are robust tools for measuring extracellular HA transmission in both physiological and pathological processes.",

keywords = "genetically encoded sensor, GRAB sensor, histamine, sleep-wake cycle",

author = "Hui Dong and Mengyao Li and Yuqi Yan and Tongrui Qian and Yunzhi Lin and Xiaoyuan Ma and Vischer, {Henry F.} and Can Liu and Guochuan Li and Huan Wang and Rob Leurs and Yulong Li",

note = "Funding Information: This research was supported by grants to Y.L. from the National Natural Science Foundation of China (31925017), the National Key R&D Program of China ( 2019YFE011781 ), the NIH BRAIN Initiative ( 1U01NS113358 and 1U01NS120824 ), the Beijing Municipal Science & Technology Commission ( Z220009 ), the Feng Foundation of Biomedical Research , the Clement and Xinxin Foundation , the Peking-Tsinghua Center for Life Sciences , and the State Key Laboratory of Membrane Biology at School of Life Sciences , Peking University . We thank Dr. Yi Rao for sharing the two-photon microscope and Dr. Xiaoguang Lei at PKU-CLS and the National Center for Protein Sciences at Peking University for providing support for the Opera Phenix high-content screening system and imaging platform. We thank Dr. Xiangdong Yang at Fudan University, who kindly provided HDC KO mice. Some graphics were generated using BioRender.com . Funding Information: This research was supported by grants to Y.L. from the National Natural Science Foundation of China (31925017), the National Key R&D Program of China (2019YFE011781), the NIH BRAIN Initiative (1U01NS113358 and 1U01NS120824), the Beijing Municipal Science & Technology Commission (Z220009), the Feng Foundation of Biomedical Research, the Clement and Xinxin Foundation, the Peking-Tsinghua Center for Life Sciences, and the State Key Laboratory of Membrane Biology at School of Life Sciences, Peking University. We thank Dr. Yi Rao for sharing the two-photon microscope and Dr. Xiaoguang Lei at PKU-CLS and the National Center for Protein Sciences at Peking University for providing support for the Opera Phenix high-content screening system and imaging platform. We thank Dr. Xiangdong Yang at Fudan University, who kindly provided HDC KO mice. Some graphics were generated using BioRender.com. Y.L. conceived and supervised the project. M.L. performed the experiments related to developing, optimizing, and characterizing the sensor in cultured HEK293T cells and neurons. Y.Y. characterized HA sensors in HEK293T cells and neurons. X.M. and H.F.V. performed the binding studies. T.Q. and M.L. performed the experiments in brain slices. H.D. Y.L. and C.L. performed the in vivo recording in freely behaving mice. G.L. and H.W. performed the characterization of the wavelength spectra of HA sensors in HEK293T cells. All authors contributed to data interpretation and analysis. Y.L. H.D. and Y.Y. wrote the manuscript with input from all other authors. Y.L. has filed patent applications, the value of which might be affected by this publication. We support inclusive, diverse, and equitable conduct of research. Publisher Copyright: {\textcopyright} 2023 Elsevier Inc.",

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AU - Ma, Xiaoyuan

AU - Vischer, Henry F.

AU - Liu, Can

AU - Li, Guochuan

AU - Wang, Huan

AU - Leurs, Rob

AU - Li, Yulong

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N2 - Histamine (HA) is a key biogenic monoamine involved in a wide range of physiological and pathological processes in both the central and peripheral nervous systems. Because the ability to directly measure extracellular HA in real time will provide important insights into the functional role of HA in complex circuits under a variety of conditions, we developed a series of genetically encoded G-protein-coupled receptor-activation-based (GRAB) HA (GRABHA) sensors with good photostability, sub-second kinetics, nanomolar affinity, and high specificity. Using these GRABHA sensors, we measured electrical-stimulation-evoked HA release in acute brain slices with high spatiotemporal resolution. Moreover, we recorded HA release in the preoptic area of the hypothalamus and prefrontal cortex during the sleep-wake cycle in freely moving mice, finding distinct patterns of HA dynamics between these specific brain regions. Thus, GRABHA sensors are robust tools for measuring extracellular HA transmission in both physiological and pathological processes.

AB - Histamine (HA) is a key biogenic monoamine involved in a wide range of physiological and pathological processes in both the central and peripheral nervous systems. Because the ability to directly measure extracellular HA in real time will provide important insights into the functional role of HA in complex circuits under a variety of conditions, we developed a series of genetically encoded G-protein-coupled receptor-activation-based (GRAB) HA (GRABHA) sensors with good photostability, sub-second kinetics, nanomolar affinity, and high specificity. Using these GRABHA sensors, we measured electrical-stimulation-evoked HA release in acute brain slices with high spatiotemporal resolution. Moreover, we recorded HA release in the preoptic area of the hypothalamus and prefrontal cortex during the sleep-wake cycle in freely moving mice, finding distinct patterns of HA dynamics between these specific brain regions. Thus, GRABHA sensors are robust tools for measuring extracellular HA transmission in both physiological and pathological processes.

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Genetically encoded sensors for measuring histamine release both in vitro and in vivo

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