Near-Infrared Voltage Nanosensors Enable Real-Time Imaging of Neuronal Activities in Mice and Zebrafish
Optical voltage sensors with the ability to monitor neuronal activities are invaluable tools for studying information processing of the brain. However, the current genetically encoded voltage indicators usually require high-power visible light for excitation and are limited to genetically addressabl...
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| Veröffentlicht in: | Journal of the American Chemical Society 2020-04, Vol.142 (17), p.7858-7867 |
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| container_title | Journal of the American Chemical Society |
| container_volume | 142 |
| creator | Liu, Jianan Zhang, Rongwei Shang, Chunfeng Zhang, Yu Feng, Yun Pan, Limin Xu, Bing Hyeon, Taeghwan Bu, Wenbo Shi, Jianlin Du, Jiulin |
| description | Optical voltage sensors with the ability to monitor neuronal activities are invaluable tools for studying information processing of the brain. However, the current genetically encoded voltage indicators usually require high-power visible light for excitation and are limited to genetically addressable model animals. Here, we report a near-infrared (NIR)-excited nongenetic voltage nanosensor that achieves stable recording of neuronal membrane potential in intact animals. The nanosensor is composed of a Förster resonance energy transfer (FRET) pair, the outer membrane-anchored upconversion nanoparticle (UCNP), and the membrane-embedded dipicrylamine (DPA). The negative charge of DPA allows membrane potential fluctuation to affect the distance between the DPA and UCNP, therefore changing the FRET efficiency. Consequently, the emission intensity of the nanosensor can report the membrane potential. Using the nanosensor, we monitor not only electrically evoked changes in the membrane potential of cultured cells but also sensory responses of neurons in intact zebrafish and brain state-modulated subthreshold activities of cortical neurons in intact mice. |
| doi_str_mv | 10.1021/jacs.0c01025 |
| format | Article |
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Using the nanosensor, we monitor not only electrically evoked changes in the membrane potential of cultured cells but also sensory responses of neurons in intact zebrafish and brain state-modulated subthreshold activities of cortical neurons in intact mice.</description><identifier>ISSN: 0002-7863</identifier><identifier>EISSN: 1520-5126</identifier><identifier>DOI: 10.1021/jacs.0c01025</identifier><identifier>PMID: 32259437</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Animals ; Fluorescence Resonance Energy Transfer - methods ; Mice ; Nanotechnology - methods ; Neurons - metabolism ; Spectroscopy, Near-Infrared - methods ; Zebrafish</subject><ispartof>Journal of the American Chemical Society, 2020-04, Vol.142 (17), p.7858-7867</ispartof><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a324t-9f108140ea9685a3011fd92cb8a39b90e12d26cf01147a329a4de7b126c4ff4b3</citedby><cites>FETCH-LOGICAL-a324t-9f108140ea9685a3011fd92cb8a39b90e12d26cf01147a329a4de7b126c4ff4b3</cites><orcidid>0000-0001-5959-6257 ; 0000-0001-8790-195X ; 0000-0001-6664-3453 ; 0000-0002-2953-4562</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/jacs.0c01025$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/jacs.0c01025$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,780,784,2765,27076,27924,27925,56738,56788</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32259437$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Jianan</creatorcontrib><creatorcontrib>Zhang, Rongwei</creatorcontrib><creatorcontrib>Shang, Chunfeng</creatorcontrib><creatorcontrib>Zhang, Yu</creatorcontrib><creatorcontrib>Feng, Yun</creatorcontrib><creatorcontrib>Pan, Limin</creatorcontrib><creatorcontrib>Xu, Bing</creatorcontrib><creatorcontrib>Hyeon, Taeghwan</creatorcontrib><creatorcontrib>Bu, Wenbo</creatorcontrib><creatorcontrib>Shi, Jianlin</creatorcontrib><creatorcontrib>Du, Jiulin</creatorcontrib><title>Near-Infrared Voltage Nanosensors Enable Real-Time Imaging of Neuronal Activities in Mice and Zebrafish</title><title>Journal of the American Chemical Society</title><addtitle>J. Am. Chem. Soc</addtitle><description>Optical voltage sensors with the ability to monitor neuronal activities are invaluable tools for studying information processing of the brain. However, the current genetically encoded voltage indicators usually require high-power visible light for excitation and are limited to genetically addressable model animals. Here, we report a near-infrared (NIR)-excited nongenetic voltage nanosensor that achieves stable recording of neuronal membrane potential in intact animals. The nanosensor is composed of a Förster resonance energy transfer (FRET) pair, the outer membrane-anchored upconversion nanoparticle (UCNP), and the membrane-embedded dipicrylamine (DPA). The negative charge of DPA allows membrane potential fluctuation to affect the distance between the DPA and UCNP, therefore changing the FRET efficiency. Consequently, the emission intensity of the nanosensor can report the membrane potential. Using the nanosensor, we monitor not only electrically evoked changes in the membrane potential of cultured cells but also sensory responses of neurons in intact zebrafish and brain state-modulated subthreshold activities of cortical neurons in intact mice.</description><subject>Animals</subject><subject>Fluorescence Resonance Energy Transfer - methods</subject><subject>Mice</subject><subject>Nanotechnology - methods</subject><subject>Neurons - metabolism</subject><subject>Spectroscopy, Near-Infrared - methods</subject><subject>Zebrafish</subject><issn>0002-7863</issn><issn>1520-5126</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNptkEtPwzAQhC0EouVx44x85ECK7TivY4V4VCpFQoUDl2jjrIurxC52gsS_JxUFLpxWs5qZ1X6EnHE24UzwqzWoMGGKDSLZI2OeCBYlXKT7ZMwYE1GWp_GIHIWwHqQUOT8ko1iIpJBxNiarBYKPZlZ78FjTF9d0sEK6AOsC2uB8oDcWqgbpE0ITLU2LdNbCytgVdZousPfOQkOnqjMfpjMYqLH0wSikYGv6ipUHbcLbCTnQ0AQ83c1j8nx7s7y-j-aPd7Pr6TyCWMguKjRnOZcMoUjzBGLGua4Loaoc4qIqGHJRi1TpYS-zIVKArDGrhneV1FpW8TG5-O7dePfeY-jK1gSFTQMWXR9KEedZKtMizwbr5bdVeReCR11uvGnBf5aclVu05RZtuUM72M93zX3VYv1r_mH5d3qbWrveD1zC_11f1sKBRg</recordid><startdate>20200429</startdate><enddate>20200429</enddate><creator>Liu, Jianan</creator><creator>Zhang, Rongwei</creator><creator>Shang, Chunfeng</creator><creator>Zhang, Yu</creator><creator>Feng, Yun</creator><creator>Pan, Limin</creator><creator>Xu, Bing</creator><creator>Hyeon, Taeghwan</creator><creator>Bu, Wenbo</creator><creator>Shi, Jianlin</creator><creator>Du, Jiulin</creator><general>American Chemical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5959-6257</orcidid><orcidid>https://orcid.org/0000-0001-8790-195X</orcidid><orcidid>https://orcid.org/0000-0001-6664-3453</orcidid><orcidid>https://orcid.org/0000-0002-2953-4562</orcidid></search><sort><creationdate>20200429</creationdate><title>Near-Infrared Voltage Nanosensors Enable Real-Time Imaging of Neuronal Activities in Mice and Zebrafish</title><author>Liu, Jianan ; Zhang, Rongwei ; Shang, Chunfeng ; Zhang, Yu ; Feng, Yun ; Pan, Limin ; Xu, Bing ; Hyeon, Taeghwan ; Bu, Wenbo ; Shi, Jianlin ; Du, Jiulin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a324t-9f108140ea9685a3011fd92cb8a39b90e12d26cf01147a329a4de7b126c4ff4b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Fluorescence Resonance Energy Transfer - methods</topic><topic>Mice</topic><topic>Nanotechnology - methods</topic><topic>Neurons - metabolism</topic><topic>Spectroscopy, Near-Infrared - methods</topic><topic>Zebrafish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Jianan</creatorcontrib><creatorcontrib>Zhang, Rongwei</creatorcontrib><creatorcontrib>Shang, Chunfeng</creatorcontrib><creatorcontrib>Zhang, Yu</creatorcontrib><creatorcontrib>Feng, Yun</creatorcontrib><creatorcontrib>Pan, Limin</creatorcontrib><creatorcontrib>Xu, Bing</creatorcontrib><creatorcontrib>Hyeon, Taeghwan</creatorcontrib><creatorcontrib>Bu, Wenbo</creatorcontrib><creatorcontrib>Shi, Jianlin</creatorcontrib><creatorcontrib>Du, Jiulin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of the American Chemical Society</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Jianan</au><au>Zhang, Rongwei</au><au>Shang, Chunfeng</au><au>Zhang, Yu</au><au>Feng, Yun</au><au>Pan, Limin</au><au>Xu, Bing</au><au>Hyeon, Taeghwan</au><au>Bu, Wenbo</au><au>Shi, Jianlin</au><au>Du, Jiulin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Near-Infrared Voltage Nanosensors Enable Real-Time Imaging of Neuronal Activities in Mice and Zebrafish</atitle><jtitle>Journal of the American Chemical Society</jtitle><addtitle>J. Am. Chem. Soc</addtitle><date>2020-04-29</date><risdate>2020</risdate><volume>142</volume><issue>17</issue><spage>7858</spage><epage>7867</epage><pages>7858-7867</pages><issn>0002-7863</issn><eissn>1520-5126</eissn><abstract>Optical voltage sensors with the ability to monitor neuronal activities are invaluable tools for studying information processing of the brain. However, the current genetically encoded voltage indicators usually require high-power visible light for excitation and are limited to genetically addressable model animals. Here, we report a near-infrared (NIR)-excited nongenetic voltage nanosensor that achieves stable recording of neuronal membrane potential in intact animals. The nanosensor is composed of a Förster resonance energy transfer (FRET) pair, the outer membrane-anchored upconversion nanoparticle (UCNP), and the membrane-embedded dipicrylamine (DPA). The negative charge of DPA allows membrane potential fluctuation to affect the distance between the DPA and UCNP, therefore changing the FRET efficiency. Consequently, the emission intensity of the nanosensor can report the membrane potential. Using the nanosensor, we monitor not only electrically evoked changes in the membrane potential of cultured cells but also sensory responses of neurons in intact zebrafish and brain state-modulated subthreshold activities of cortical neurons in intact mice.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>32259437</pmid><doi>10.1021/jacs.0c01025</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-5959-6257</orcidid><orcidid>https://orcid.org/0000-0001-8790-195X</orcidid><orcidid>https://orcid.org/0000-0001-6664-3453</orcidid><orcidid>https://orcid.org/0000-0002-2953-4562</orcidid></addata></record> |
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| subjects | Animals Fluorescence Resonance Energy Transfer - methods Mice Nanotechnology - methods Neurons - metabolism Spectroscopy, Near-Infrared - methods Zebrafish |
| title | Near-Infrared Voltage Nanosensors Enable Real-Time Imaging of Neuronal Activities in Mice and Zebrafish |
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