Probing Neuropeptide Volume Transmission In Vivo by Simultaneous Near-Infrared Light-Triggered Release and Optical Sensing**

Hejian Xiong; Emre Lacin; Hui Ouyang; Aditi Naik; Xueqi Xu; Chen Xie; Jonghae Youn; Blake A. Wilson; Krutin Kumar; Tyler Kern; Erin Aisenberg; Daniel Kircher; Xiuying Li; Joseph A. Zasadzinski; Celine Mateo; David Kleinfeld; Sabina Hrabetova; Paul A. Slesinger; Zhenpeng Qin

doi:10.1002/anie.202206122

Probing Neuropeptide Volume Transmission In Vivo by Simultaneous Near-Infrared Light-Triggered Release and Optical Sensing**

Hejian Xiong, Emre Lacin, Hui Ouyang, Aditi Naik, Xueqi Xu, Chen Xie, Jonghae Youn, Blake A. Wilson, Krutin Kumar, Tyler Kern, Erin Aisenberg, Daniel Kircher, Xiuying Li, Joseph A. Zasadzinski, Celine Mateo, David Kleinfeld, Sabina Hrabetova, Paul A. Slesinger, Zhenpeng Qin

Research output: Contribution to journal › Article › peer-review

24 Scopus citations

Abstract

Neuropeptides are abundant signaling molecules in the central nervous system. Yet remarkably little is known about their spatiotemporal spread and biological activity. Here, we developed an integrated optical approach using Plasmonic nAnovesicles and cell-based neurotransmitter fluorescent engineered reporter (CNiFER), or PACE, to probe neuropeptide signaling in the mouse neocortex. Small volumes (fL to pL) of exogenously supplied somatostatin-14 (SST) can be rapidly released under near-infrared light stimulation from nanovesicles implanted in the brain and detected by SST2 CNiFERs with nM sensitivity. Our measurements reveal reduced but synchronized SST transmission within 130 μm, and markedly smaller and delayed transmission at longer distances. These measurements enabled a quantitative estimation of the SST loss rate due to peptide degradation and binding. PACE offers a new tool for determining the spatiotemporal scales of neuropeptide volume transmission and signaling in the brain.

Original language	English (US)
Article number	e202206122
Journal	Angewandte Chemie - International Edition
Volume	61
Issue number	34
DOIs	https://doi.org/10.1002/anie.202206122
State	Published - Aug 22 2022
Externally published	Yes

Bibliographical note

Funding Information:
We thank Dr. Oliver Griesbeck for providing the Twitch2B cDNA clone and discussions. Schematic figures were made with BioRender.com. This work was partially supported by National Science Foundation under award number 1631910 (Z.Q.), National Institute of Neurological Disorders and Stroke of the National Institutes of Health (NIH) under award number RF1NS110499 (Z.Q., P.A.S.), National Institute of Mental Health of NIH under award number R01MH111499 (P.A.S.), Human Frontier Science Program (HFSP) under award RGP0036/2020 (S.H.), and a postdoc research grant from the Phospholipid Research Center (Heidelberg, Germany) to H.X.

Publisher Copyright:
© 2022 Wiley-VCH GmbH.

Keywords

Biosensors
Brain
Neuropeptide Release
Neuropeptide Transmission
Plasmonic Nanovesicles
Somatostatin/metabolism
Animals
Signal Transduction
Neuropeptides
Mice
Brain/metabolism

PubMed: MeSH publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Journal Article
Research Support, N.I.H., Extramural

Publisher link

10.1002/anie.202206122

Find It

Find It at U of M Libraries

Cite this

Xiong, H., Lacin, E., Ouyang, H., Naik, A., Xu, X., Xie, C., Youn, J., Wilson, B. A., Kumar, K., Kern, T., Aisenberg, E., Kircher, D., Li, X., Zasadzinski, J. A., Mateo, C., Kleinfeld, D., Hrabetova, S., Slesinger, P. A., & Qin, Z. (2022). Probing Neuropeptide Volume Transmission In Vivo by Simultaneous Near-Infrared Light-Triggered Release and Optical Sensing**. Angewandte Chemie - International Edition, 61(34), Article e202206122. https://doi.org/10.1002/anie.202206122

Xiong, H, Lacin, E, Ouyang, H, Naik, A, Xu, X, Xie, C, Youn, J, Wilson, BA, Kumar, K, Kern, T, Aisenberg, E, Kircher, D, Li, X, Zasadzinski, JA, Mateo, C, Kleinfeld, D, Hrabetova, S, Slesinger, PA & Qin, Z 2022, 'Probing Neuropeptide Volume Transmission In Vivo by Simultaneous Near-Infrared Light-Triggered Release and Optical Sensing**', Angewandte Chemie - International Edition, vol. 61, no. 34, e202206122. https://doi.org/10.1002/anie.202206122

@article{3e270a471e85404da507da96dc140885,

title = "Probing Neuropeptide Volume Transmission In Vivo by Simultaneous Near-Infrared Light-Triggered Release and Optical Sensing**",

abstract = "Neuropeptides are abundant signaling molecules in the central nervous system. Yet remarkably little is known about their spatiotemporal spread and biological activity. Here, we developed an integrated optical approach using Plasmonic nAnovesicles and cell-based neurotransmitter fluorescent engineered reporter (CNiFER), or PACE, to probe neuropeptide signaling in the mouse neocortex. Small volumes (fL to pL) of exogenously supplied somatostatin-14 (SST) can be rapidly released under near-infrared light stimulation from nanovesicles implanted in the brain and detected by SST2 CNiFERs with nM sensitivity. Our measurements reveal reduced but synchronized SST transmission within 130 μm, and markedly smaller and delayed transmission at longer distances. These measurements enabled a quantitative estimation of the SST loss rate due to peptide degradation and binding. PACE offers a new tool for determining the spatiotemporal scales of neuropeptide volume transmission and signaling in the brain.",

keywords = "Biosensors, Brain, Neuropeptide Release, Neuropeptide Transmission, Plasmonic Nanovesicles, Somatostatin/metabolism, Animals, Signal Transduction, Neuropeptides, Mice, Brain/metabolism",

author = "Hejian Xiong and Emre Lacin and Hui Ouyang and Aditi Naik and Xueqi Xu and Chen Xie and Jonghae Youn and Wilson, {Blake A.} and Krutin Kumar and Tyler Kern and Erin Aisenberg and Daniel Kircher and Xiuying Li and Zasadzinski, {Joseph A.} and Celine Mateo and David Kleinfeld and Sabina Hrabetova and Slesinger, {Paul A.} and Zhenpeng Qin",

note = "Funding Information: We thank Dr. Oliver Griesbeck for providing the Twitch2B cDNA clone and discussions. Schematic figures were made with BioRender.com. This work was partially supported by National Science Foundation under award number 1631910 (Z.Q.), National Institute of Neurological Disorders and Stroke of the National Institutes of Health (NIH) under award number RF1NS110499 (Z.Q., P.A.S.), National Institute of Mental Health of NIH under award number R01MH111499 (P.A.S.), Human Frontier Science Program (HFSP) under award RGP0036/2020 (S.H.), and a postdoc research grant from the Phospholipid Research Center (Heidelberg, Germany) to H.X. Publisher Copyright: {\textcopyright} 2022 Wiley-VCH GmbH.",

year = "2022",

month = aug,

day = "22",

doi = "10.1002/anie.202206122",

language = "English (US)",

volume = "61",

journal = "Angewandte Chemie - International Edition",

issn = "1433-7851",

publisher = "John Wiley and Sons Ltd",

number = "34",

}

TY - JOUR

T1 - Probing Neuropeptide Volume Transmission In Vivo by Simultaneous Near-Infrared Light-Triggered Release and Optical Sensing**

AU - Xiong, Hejian

AU - Lacin, Emre

AU - Ouyang, Hui

AU - Naik, Aditi

AU - Xu, Xueqi

AU - Xie, Chen

AU - Youn, Jonghae

AU - Wilson, Blake A.

AU - Kumar, Krutin

AU - Kern, Tyler

AU - Aisenberg, Erin

AU - Kircher, Daniel

AU - Li, Xiuying

AU - Zasadzinski, Joseph A.

AU - Mateo, Celine

AU - Kleinfeld, David

AU - Hrabetova, Sabina

AU - Slesinger, Paul A.

AU - Qin, Zhenpeng

N1 - Funding Information: We thank Dr. Oliver Griesbeck for providing the Twitch2B cDNA clone and discussions. Schematic figures were made with BioRender.com. This work was partially supported by National Science Foundation under award number 1631910 (Z.Q.), National Institute of Neurological Disorders and Stroke of the National Institutes of Health (NIH) under award number RF1NS110499 (Z.Q., P.A.S.), National Institute of Mental Health of NIH under award number R01MH111499 (P.A.S.), Human Frontier Science Program (HFSP) under award RGP0036/2020 (S.H.), and a postdoc research grant from the Phospholipid Research Center (Heidelberg, Germany) to H.X. Publisher Copyright: © 2022 Wiley-VCH GmbH.

PY - 2022/8/22

Y1 - 2022/8/22

N2 - Neuropeptides are abundant signaling molecules in the central nervous system. Yet remarkably little is known about their spatiotemporal spread and biological activity. Here, we developed an integrated optical approach using Plasmonic nAnovesicles and cell-based neurotransmitter fluorescent engineered reporter (CNiFER), or PACE, to probe neuropeptide signaling in the mouse neocortex. Small volumes (fL to pL) of exogenously supplied somatostatin-14 (SST) can be rapidly released under near-infrared light stimulation from nanovesicles implanted in the brain and detected by SST2 CNiFERs with nM sensitivity. Our measurements reveal reduced but synchronized SST transmission within 130 μm, and markedly smaller and delayed transmission at longer distances. These measurements enabled a quantitative estimation of the SST loss rate due to peptide degradation and binding. PACE offers a new tool for determining the spatiotemporal scales of neuropeptide volume transmission and signaling in the brain.

AB - Neuropeptides are abundant signaling molecules in the central nervous system. Yet remarkably little is known about their spatiotemporal spread and biological activity. Here, we developed an integrated optical approach using Plasmonic nAnovesicles and cell-based neurotransmitter fluorescent engineered reporter (CNiFER), or PACE, to probe neuropeptide signaling in the mouse neocortex. Small volumes (fL to pL) of exogenously supplied somatostatin-14 (SST) can be rapidly released under near-infrared light stimulation from nanovesicles implanted in the brain and detected by SST2 CNiFERs with nM sensitivity. Our measurements reveal reduced but synchronized SST transmission within 130 μm, and markedly smaller and delayed transmission at longer distances. These measurements enabled a quantitative estimation of the SST loss rate due to peptide degradation and binding. PACE offers a new tool for determining the spatiotemporal scales of neuropeptide volume transmission and signaling in the brain.

KW - Biosensors

KW - Brain

KW - Neuropeptide Release

KW - Neuropeptide Transmission

KW - Plasmonic Nanovesicles

KW - Somatostatin/metabolism

KW - Animals

KW - Signal Transduction

KW - Neuropeptides

KW - Mice

KW - Brain/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85133609608&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85133609608&partnerID=8YFLogxK

U2 - 10.1002/anie.202206122

DO - 10.1002/anie.202206122

M3 - Article

C2 - 35723610

AN - SCOPUS:85133609608

SN - 1433-7851

VL - 61

JO - Angewandte Chemie - International Edition

JF - Angewandte Chemie - International Edition

IS - 34

M1 - e202206122

ER -

Probing Neuropeptide Volume Transmission In Vivo by Simultaneous Near-Infrared Light-Triggered Release and Optical Sensing**

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

Publisher link

Find It

Other files and links

Fingerprint

Cite this