A genetically encoded far‐red fluorescent calcium ion biosensor derived from a biliverdin‐binding protein
Far‐red and near‐infrared (NIR) genetically encoded calcium ion (Ca2+) indicators (GECIs) are powerful tools for in vivo and multiplexed imaging of neural activity and cell signaling. Inspired by a previous report to engineer a far‐red fluorescent protein (FP) from a biliverdin (BV)‐binding NIR FP,...
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| Published in | Protein science Vol. 31; no. 10; pp. e4440 - n/a |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Hoboken, USA
John Wiley & Sons, Inc
01.10.2022
Wiley Subscription Services, Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0961-8368 1469-896X 1469-896X |
| DOI | 10.1002/pro.4440 |
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| Abstract | Far‐red and near‐infrared (NIR) genetically encoded calcium ion (Ca2+) indicators (GECIs) are powerful tools for in vivo and multiplexed imaging of neural activity and cell signaling. Inspired by a previous report to engineer a far‐red fluorescent protein (FP) from a biliverdin (BV)‐binding NIR FP, we have developed a far‐red fluorescent GECI, designated iBB‐GECO1, from a previously reported NIR GECI. iBB‐GECO1 exhibits a relatively high molecular brightness, an inverse response to Ca2+ with ΔF/Fmin = −13, and a near‐optimal dissociation constant (Kd) for Ca2+ of 105 nM. We demonstrate the utility of iBB‐GECO1 for four‐color multiplexed imaging in MIN6 cells and five‐color imaging in HEK293T cells. Like other BV‐binding GECIs, iBB‐GECO1 did not give robust signals during in vivo imaging of neural activity in mice, but did provide promising results that will guide future engineering efforts.
Significance
Genetically encoded calcium ion (Ca2+) indicators (GECIs) compatible with common far‐red laser lines (~630–640 nm) on commercial microscopes are of critical importance for their widespread application to deep‐tissue multiplexed imaging of neural activity. In this study, we engineered a far‐red excitable fluorescent GECI, designated iBB‐GECO1, that exhibits a range of preferable specifications such as high brightness, large fluorescence response to Ca2+, and compatibility with multiplexed imaging in mammalian cells. |
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| AbstractList | Far‐red and near‐infrared (NIR) genetically encoded calcium ion (Ca2+) indicators (GECIs) are powerful tools for in vivo and multiplexed imaging of neural activity and cell signaling. Inspired by a previous report to engineer a far‐red fluorescent protein (FP) from a biliverdin (BV)‐binding NIR FP, we have developed a far‐red fluorescent GECI, designated iBB‐GECO1, from a previously reported NIR GECI. iBB‐GECO1 exhibits a relatively high molecular brightness, an inverse response to Ca2+ with ΔF/F
min = −13, and a near‐optimal dissociation constant (K
d) for Ca2+ of 105 nM. We demonstrate the utility of iBB‐GECO1 for four‐color multiplexed imaging in MIN6 cells and five‐color imaging in HEK293T cells. Like other BV‐binding GECIs, iBB‐GECO1 did not give robust signals during in vivo imaging of neural activity in mice, but did provide promising results that will guide future engineering efforts. Far‐red and near‐infrared (NIR) genetically encoded calcium ion (Ca2+) indicators (GECIs) are powerful tools for in vivo and multiplexed imaging of neural activity and cell signaling. Inspired by a previous report to engineer a far‐red fluorescent protein (FP) from a biliverdin (BV)‐binding NIR FP, we have developed a far‐red fluorescent GECI, designated iBB‐GECO1, from a previously reported NIR GECI. iBB‐GECO1 exhibits a relatively high molecular brightness, an inverse response to Ca2+ with ΔF/Fmin = −13, and a near‐optimal dissociation constant (Kd) for Ca2+ of 105 nM. We demonstrate the utility of iBB‐GECO1 for four‐color multiplexed imaging in MIN6 cells and five‐color imaging in HEK293T cells. Like other BV‐binding GECIs, iBB‐GECO1 did not give robust signals during in vivo imaging of neural activity in mice, but did provide promising results that will guide future engineering efforts. Significance Genetically encoded calcium ion (Ca2+) indicators (GECIs) compatible with common far‐red laser lines (~630–640 nm) on commercial microscopes are of critical importance for their widespread application to deep‐tissue multiplexed imaging of neural activity. In this study, we engineered a far‐red excitable fluorescent GECI, designated iBB‐GECO1, that exhibits a range of preferable specifications such as high brightness, large fluorescence response to Ca2+, and compatibility with multiplexed imaging in mammalian cells. Far-red and near-infrared (NIR) genetically encoded calcium ion (Ca2+ ) indicators (GECIs) are powerful tools for in vivo and multiplexed imaging of neural activity and cell signaling. Inspired by a previous report to engineer a far-red fluorescent protein (FP) from a biliverdin (BV)-binding NIR FP, we have developed a far-red fluorescent GECI, designated iBB-GECO1, from a previously reported NIR GECI. iBB-GECO1 exhibits a relatively high molecular brightness, an inverse response to Ca2+ with ΔF/Fmin = -13, and a near-optimal dissociation constant (Kd ) for Ca2+ of 105 nM. We demonstrate the utility of iBB-GECO1 for four-color multiplexed imaging in MIN6 cells and five-color imaging in HEK293T cells. Like other BV-binding GECIs, iBB-GECO1 did not give robust signals during in vivo imaging of neural activity in mice, but did provide promising results that will guide future engineering efforts. SIGNIFICANCE: Genetically encoded calcium ion (Ca2+ ) indicators (GECIs) compatible with common far-red laser lines (~630-640 nm) on commercial microscopes are of critical importance for their widespread application to deep-tissue multiplexed imaging of neural activity. In this study, we engineered a far-red excitable fluorescent GECI, designated iBB-GECO1, that exhibits a range of preferable specifications such as high brightness, large fluorescence response to Ca2+ , and compatibility with multiplexed imaging in mammalian cells.Far-red and near-infrared (NIR) genetically encoded calcium ion (Ca2+ ) indicators (GECIs) are powerful tools for in vivo and multiplexed imaging of neural activity and cell signaling. Inspired by a previous report to engineer a far-red fluorescent protein (FP) from a biliverdin (BV)-binding NIR FP, we have developed a far-red fluorescent GECI, designated iBB-GECO1, from a previously reported NIR GECI. iBB-GECO1 exhibits a relatively high molecular brightness, an inverse response to Ca2+ with ΔF/Fmin = -13, and a near-optimal dissociation constant (Kd ) for Ca2+ of 105 nM. We demonstrate the utility of iBB-GECO1 for four-color multiplexed imaging in MIN6 cells and five-color imaging in HEK293T cells. Like other BV-binding GECIs, iBB-GECO1 did not give robust signals during in vivo imaging of neural activity in mice, but did provide promising results that will guide future engineering efforts. SIGNIFICANCE: Genetically encoded calcium ion (Ca2+ ) indicators (GECIs) compatible with common far-red laser lines (~630-640 nm) on commercial microscopes are of critical importance for their widespread application to deep-tissue multiplexed imaging of neural activity. In this study, we engineered a far-red excitable fluorescent GECI, designated iBB-GECO1, that exhibits a range of preferable specifications such as high brightness, large fluorescence response to Ca2+ , and compatibility with multiplexed imaging in mammalian cells. Far‐red and near‐infrared (NIR) genetically encoded calcium ion (Ca2+) indicators (GECIs) are powerful tools for in vivo and multiplexed imaging of neural activity and cell signaling. Inspired by a previous report to engineer a far‐red fluorescent protein (FP) from a biliverdin (BV)‐binding NIR FP, we have developed a far‐red fluorescent GECI, designated iBB‐GECO1, from a previously reported NIR GECI. iBB‐GECO1 exhibits a relatively high molecular brightness, an inverse response to Ca2+ with ΔF/Fmin = −13, and a near‐optimal dissociation constant (Kd) for Ca2+ of 105 nM. We demonstrate the utility of iBB‐GECO1 for four‐color multiplexed imaging in MIN6 cells and five‐color imaging in HEK293T cells. Like other BV‐binding GECIs, iBB‐GECO1 did not give robust signals during in vivo imaging of neural activity in mice, but did provide promising results that will guide future engineering efforts.SignificanceGenetically encoded calcium ion (Ca2+) indicators (GECIs) compatible with common far‐red laser lines (~630–640 nm) on commercial microscopes are of critical importance for their widespread application to deep‐tissue multiplexed imaging of neural activity. In this study, we engineered a far‐red excitable fluorescent GECI, designated iBB‐GECO1, that exhibits a range of preferable specifications such as high brightness, large fluorescence response to Ca2+, and compatibility with multiplexed imaging in mammalian cells. Far-red and near-infrared (NIR) genetically encoded calcium ion (Ca ) indicators (GECIs) are powerful tools for in vivo and multiplexed imaging of neural activity and cell signaling. Inspired by a previous report to engineer a far-red fluorescent protein (FP) from a biliverdin (BV)-binding NIR FP, we have developed a far-red fluorescent GECI, designated iBB-GECO1, from a previously reported NIR GECI. iBB-GECO1 exhibits a relatively high molecular brightness, an inverse response to Ca with ΔF/F = -13, and a near-optimal dissociation constant (K ) for Ca of 105 nM. We demonstrate the utility of iBB-GECO1 for four-color multiplexed imaging in MIN6 cells and five-color imaging in HEK293T cells. Like other BV-binding GECIs, iBB-GECO1 did not give robust signals during in vivo imaging of neural activity in mice, but did provide promising results that will guide future engineering efforts. SIGNIFICANCE: Genetically encoded calcium ion (Ca ) indicators (GECIs) compatible with common far-red laser lines (~630-640 nm) on commercial microscopes are of critical importance for their widespread application to deep-tissue multiplexed imaging of neural activity. In this study, we engineered a far-red excitable fluorescent GECI, designated iBB-GECO1, that exhibits a range of preferable specifications such as high brightness, large fluorescence response to Ca , and compatibility with multiplexed imaging in mammalian cells. |
| Author | Ota, Keisuke Hashizume, Rina Zhu, Wenchao Zhang, Jin Campbell, Robert E. Mehta, Sohum Drobizhev, Mikhail Fujii, Hajime Qian, Yong Bito, Haruhiko Nasu, Yusuke |
| AuthorAffiliation | 3 Department of Pharmacology University of California San Diego La Jolla California USA 2 Department of Neurochemistry, Graduate School of Medicine The University of Tokyo, Bunkyo‐ku Tokyo Japan 1 Department of Chemistry, School of Science The University of Tokyo, Bunkyo‐ku Tokyo Japan 6 Department of Microbiology and Cell Biology Montana State University Bozeman Montana USA 4 Department of Chemistry University of Alberta Edmonton Alberta Canada 5 McGovern Institute for Brain Research, MIT Cambridge Massachusetts USA |
| AuthorAffiliation_xml | – name: 1 Department of Chemistry, School of Science The University of Tokyo, Bunkyo‐ku Tokyo Japan – name: 3 Department of Pharmacology University of California San Diego La Jolla California USA – name: 2 Department of Neurochemistry, Graduate School of Medicine The University of Tokyo, Bunkyo‐ku Tokyo Japan – name: 4 Department of Chemistry University of Alberta Edmonton Alberta Canada – name: 6 Department of Microbiology and Cell Biology Montana State University Bozeman Montana USA – name: 5 McGovern Institute for Brain Research, MIT Cambridge Massachusetts USA |
| Author_xml | – sequence: 1 givenname: Rina surname: Hashizume fullname: Hashizume, Rina organization: The University of Tokyo, Bunkyo‐ku – sequence: 2 givenname: Hajime surname: Fujii fullname: Fujii, Hajime organization: The University of Tokyo, Bunkyo‐ku – sequence: 3 givenname: Sohum orcidid: 0000-0003-4764-8579 surname: Mehta fullname: Mehta, Sohum organization: University of California San Diego – sequence: 4 givenname: Keisuke surname: Ota fullname: Ota, Keisuke organization: The University of Tokyo, Bunkyo‐ku – sequence: 5 givenname: Yong orcidid: 0000-0001-7849-9022 surname: Qian fullname: Qian, Yong organization: McGovern Institute for Brain Research, MIT – sequence: 6 givenname: Wenchao surname: Zhu fullname: Zhu, Wenchao organization: The University of Tokyo, Bunkyo‐ku – sequence: 7 givenname: Mikhail surname: Drobizhev fullname: Drobizhev, Mikhail organization: Montana State University – sequence: 8 givenname: Yusuke orcidid: 0000-0002-3193-9104 surname: Nasu fullname: Nasu, Yusuke email: nasu@chem.s.u-tokyo.ac.jp organization: The University of Tokyo, Bunkyo‐ku – sequence: 9 givenname: Jin orcidid: 0000-0001-7145-7823 surname: Zhang fullname: Zhang, Jin organization: University of California San Diego – sequence: 10 givenname: Haruhiko orcidid: 0000-0001-6315-9594 surname: Bito fullname: Bito, Haruhiko organization: The University of Tokyo, Bunkyo‐ku – sequence: 11 givenname: Robert E. orcidid: 0000-0003-0604-092X surname: Campbell fullname: Campbell, Robert E. email: campbell@chem.s.u-tokyo.ac.jp organization: University of Alberta |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36173169$$D View this record in MEDLINE/PubMed |
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| Keywords | far-red fluorescence protein engineering calcium ion imaging bacterial phytochrome-derived fluorescent proteins |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Review Editor: Aitziber Cortajarena Hajime Fujii, Sohum Mehta, and Keisuke Ota contributed equally to this study. Funding information Astellas Foundation for Research on Metabolic Disorders; Canadian Institutes of Health Research; Hitachi Global Foundation; Japan Society for the Promotion of Science, Grant/Award Numbers: 19H05633, 17K13270, 22H05160; Kato Memorial Bioscience Foundation; Nakatani Foundation for Advancement of Measuring Technologies in Biomedical Engineering; National Cancer Institute, Grant/Award Number: R01 DK073368; National Institute of Neurological Disorders and Stroke, Grant/Award Number: U24 NS109107; Natural Sciences and Engineering Research Council of Canada; National Institutes of Health; Montana State University; University of Alberta; University of California, San Diego; Takeda Science Foundation; Toyota Physical and Chemical Research Institute; University of Tokyo; Japan Agency for Medical Research and Development, Grant/Award Number: 19dm0207079 |
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| SubjectTerms | Animals bacterial phytochrome‐derived fluorescent proteins Biliverdin Biliverdine - metabolism Biocompatibility Biosensing Techniques Biosensors Brightness Calcium Calcium - metabolism calcium ion imaging Calcium ions Carrier Proteins Cell signaling Color far‐red fluorescence Fluorescence Full‐length Paper Full‐length Papers Genetic code HEK293 Cells Humans Imaging Indicators Ions Luminescent Proteins - chemistry Mammalian cells Mice Microscopes Multiplexing Near infrared radiation protein engineering Proteins Red fluorescent protein |
| Title | A genetically encoded far‐red fluorescent calcium ion biosensor derived from a biliverdin‐binding protein |
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