Multiresolution Imaging Using Bioluminescence Resonance Energy Transfer Identifies Distinct Biodistribution Profiles of Extracellular Vesicles and Exomeres with Redirected Tropism

Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However, their spatiotemporal dynamics in vivo have remained largely unresolved in detail due to the lack of a suitable method. Therefore, a bioluminesce...

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Published inAdvanced science Vol. 7; no. 19; pp. 2001467 - n/a
Main Authors Wu, Anthony Yan‐Tang, Sung, Yun‐Chieh, Chen, Yen‐Ju, Chou, Steven Ting‐Yu, Guo, Vanessa, Chien, Jasper Che‐Yung, Ko, John Jun‐Sheng, Yang, Alan Ling, Huang, Hsi‐Chien, Chuang, Ju‐Chen, Wu, Syuan, Ho, Meng‐Ru, Ericsson, Maria, Lin, Wan‐Wan, Cheung, Chantal Hoi Yin, Juan, Hsueh‐Fen, Ueda, Koji, Chen, Yunching, Lai, Charles Pin‐Kuang
Format Journal Article
LanguageEnglish
Published Germany John Wiley & Sons, Inc 01.10.2020
John Wiley and Sons Inc
Wiley
Subjects
Biodistribution
Bioluminescence
bioluminescence resonance energy transfer
Communication
exomeres
exosomes
Extracellular vesicles
Labeling
Membranes
Microscopy
microvesicles
Peptides
Plasma
Proteins
redirected tropism
Tomography
Visualization
exomeres
biodistribution
bioluminescence resonance energy transfer
extracellular vesicles
exosomes
microvesicles
redirected tropism
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Abstract Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However, their spatiotemporal dynamics in vivo have remained largely unresolved in detail due to the lack of a suitable method. Therefore, a bioluminescence resonance energy transfer (BRET)‐based reporter, PalmGRET, is created to enable pan‐EP labeling ranging from exomeres (<50 nm) to small (<200 nm) and medium and large (>200 nm) EVs. PalmGRET emits robust, sustained signals and allows the visualization, tracking, and quantification of the EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, it is shown that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. It is further demonstrated that gene knockdown of lung‐tropic membrane proteins, solute carrier organic anion transporter family member 2A1, alanine aminopeptidase/Cd13, and chloride intracellular channel 1 decreases HCC‐EP distribution to the lungs and yields distinct biodistribution profiles. It is anticipated that EP‐specific imaging, quantitative assays, and detailed in vivo characterization are a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design. PalmGRET, a bioluminescence resonance energy transfer (BRET)‐based reporter for extracellular particles (EPs), enables pan‐EP labeling, including extracellular vesicles and exomeres. PalmGRET allows accurate visualization, tracking, and quantification of EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, lung‐tropic EP proteins are identified and dynamically altered biodistributions are revealed under redirected tropism.
AbstractList Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However, their spatiotemporal dynamics in vivo have remained largely unresolved in detail due to the lack of a suitable method. Therefore, a bioluminescence resonance energy transfer (BRET)‐based reporter, PalmGRET, is created to enable pan‐EP labeling ranging from exomeres (<50 nm) to small (<200 nm) and medium and large (>200 nm) EVs. PalmGRET emits robust, sustained signals and allows the visualization, tracking, and quantification of the EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, it is shown that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. It is further demonstrated that gene knockdown of lung‐tropic membrane proteins, solute carrier organic anion transporter family member 2A1, alanine aminopeptidase/Cd13, and chloride intracellular channel 1 decreases HCC‐EP distribution to the lungs and yields distinct biodistribution profiles. It is anticipated that EP‐specific imaging, quantitative assays, and detailed in vivo characterization are a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design. PalmGRET, a bioluminescence resonance energy transfer (BRET)‐based reporter for extracellular particles (EPs), enables pan‐EP labeling, including extracellular vesicles and exomeres. PalmGRET allows accurate visualization, tracking, and quantification of EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, lung‐tropic EP proteins are identified and dynamically altered biodistributions are revealed under redirected tropism.
Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However, their spatiotemporal dynamics in vivo have remained largely unresolved in detail due to the lack of a suitable method. Therefore, a bioluminescence resonance energy transfer (BRET)‐based reporter, PalmGRET, is created to enable pan‐EP labeling ranging from exomeres (<50 nm) to small (<200 nm) and medium and large (>200 nm) EVs. PalmGRET emits robust, sustained signals and allows the visualization, tracking, and quantification of the EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, it is shown that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. It is further demonstrated that gene knockdown of lung‐tropic membrane proteins, solute carrier organic anion transporter family member 2A1, alanine aminopeptidase/Cd13, and chloride intracellular channel 1 decreases HCC‐EP distribution to the lungs and yields distinct biodistribution profiles. It is anticipated that EP‐specific imaging, quantitative assays, and detailed in vivo characterization are a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design.
Abstract Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However, their spatiotemporal dynamics in vivo have remained largely unresolved in detail due to the lack of a suitable method. Therefore, a bioluminescence resonance energy transfer (BRET)‐based reporter, PalmGRET, is created to enable pan‐EP labeling ranging from exomeres (<50 nm) to small (<200 nm) and medium and large (>200 nm) EVs. PalmGRET emits robust, sustained signals and allows the visualization, tracking, and quantification of the EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, it is shown that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. It is further demonstrated that gene knockdown of lung‐tropic membrane proteins, solute carrier organic anion transporter family member 2A1, alanine aminopeptidase/Cd13, and chloride intracellular channel 1 decreases HCC‐EP distribution to the lungs and yields distinct biodistribution profiles. It is anticipated that EP‐specific imaging, quantitative assays, and detailed in vivo characterization are a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design.
Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However, their spatiotemporal dynamics in vivo have remained largely unresolved in detail due to the lack of a suitable method. Therefore, a bioluminescence resonance energy transfer (BRET)-based reporter, PalmGRET, is created to enable pan-EP labeling ranging from exomeres (<50 nm) to small (<200 nm) and medium and large (>200 nm) EVs. PalmGRET emits robust, sustained signals and allows the visualization, tracking, and quantification of the EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, it is shown that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. It is further demonstrated that gene knockdown of lung-tropic membrane proteins, solute carrier organic anion transporter family member 2A1, alanine aminopeptidase/Cd13, and chloride intracellular channel 1 decreases HCC-EP distribution to the lungs and yields distinct biodistribution profiles. It is anticipated that EP-specific imaging, quantitative assays, and detailed in vivo characterization are a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design.Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However, their spatiotemporal dynamics in vivo have remained largely unresolved in detail due to the lack of a suitable method. Therefore, a bioluminescence resonance energy transfer (BRET)-based reporter, PalmGRET, is created to enable pan-EP labeling ranging from exomeres (<50 nm) to small (<200 nm) and medium and large (>200 nm) EVs. PalmGRET emits robust, sustained signals and allows the visualization, tracking, and quantification of the EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, it is shown that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. It is further demonstrated that gene knockdown of lung-tropic membrane proteins, solute carrier organic anion transporter family member 2A1, alanine aminopeptidase/Cd13, and chloride intracellular channel 1 decreases HCC-EP distribution to the lungs and yields distinct biodistribution profiles. It is anticipated that EP-specific imaging, quantitative assays, and detailed in vivo characterization are a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design.
Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However, their spatiotemporal dynamics in vivo have remained largely unresolved in detail due to the lack of a suitable method. Therefore, a bioluminescence resonance energy transfer (BRET)‐based reporter, PalmGRET, is created to enable pan‐EP labeling ranging from exomeres (<50 nm) to small (<200 nm) and medium and large (>200 nm) EVs. PalmGRET emits robust, sustained signals and allows the visualization, tracking, and quantification of the EPs from whole animal to nanoscopic resolutions under different imaging modalities, including bioluminescence, BRET, and fluorescence. Using PalmGRET, it is shown that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. It is further demonstrated that gene knockdown of lung‐tropic membrane proteins, solute carrier organic anion transporter family member 2A1, alanine aminopeptidase/Cd13, and chloride intracellular channel 1 decreases HCC‐EP distribution to the lungs and yields distinct biodistribution profiles. It is anticipated that EP‐specific imaging, quantitative assays, and detailed in vivo characterization are a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design.
Author Chen, Yunching
Yang, Alan Ling
Ho, Meng‐Ru
Chen, Yen‐Ju
Juan, Hsueh‐Fen
Wu, Syuan
Lai, Charles Pin‐Kuang
Chou, Steven Ting‐Yu
Huang, Hsi‐Chien
Ericsson, Maria
Guo, Vanessa
Chuang, Ju‐Chen
Chien, Jasper Che‐Yung
Ko, John Jun‐Sheng
Wu, Anthony Yan‐Tang
Ueda, Koji
Cheung, Chantal Hoi Yin
Lin, Wan‐Wan
Sung, Yun‐Chieh
AuthorAffiliation 3 Department of Chemical Engineering National Tsing Hua University Hsinchu 30013 Taiwan
2 Institute of Biomedical Engineering and Frontier Research Center on Fundamental and Applied Sciences of Matters National Tsing Hua University Hsinchu 30013 Taiwan
1 Institute of Atomic and Molecular Sciences Academia Sinica Taipei 10617 Taiwan
6 Department of Pharmacology, College of Medicine National Taiwan University Taipei 100233 Taiwan
7 Department of Life Science National Taiwan University Taipei 10617 Taiwan
4 Institute of Biological Chemistry Academia Sinica Taipei 115 Taiwan
8 Cancer Proteomics Group, Cancer Precision Medicine Center Japanese Foundation for Cancer Research Tokyo 135‐8550 Japan
9 Chemical Biology and Molecular Biophysics Program Taiwan International Graduate Program Academia Sinica Taipei 11529 Taiwan
10 Genome and Systems Biology Degree Program National Taiwan University and Academia Sinica Taipei 10617 Taiwan
5 Department of Cell Biology Harvard Medical School Boston MA 02115 USA
AuthorAffiliation_xml – name: 3 Department of Chemical Engineering National Tsing Hua University Hsinchu 30013 Taiwan
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  email: laicharles@sinica.edu.tw
  organization: National Taiwan University and Academia Sinica
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33042758$$D View this record in MEDLINE/PubMed
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Issue 19
Keywords exomeres
biodistribution
bioluminescence resonance energy transfer
extracellular vesicles
exosomes
microvesicles
redirected tropism
Language English
License Attribution
2020 The Authors. Published by Wiley‐VCH GmbH.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Snippet Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications. However,...
Abstract Extracellular particles (EPs) including extracellular vesicles (EVs) and exomeres play significant roles in diseases and therapeutic applications....
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StartPage 2001467
SubjectTerms Biodistribution
Bioluminescence
bioluminescence resonance energy transfer
Communication
exomeres
exosomes
Extracellular vesicles
Labeling
Membranes
Microscopy
microvesicles
Peptides
Plasma
Proteins
redirected tropism
Tomography
Visualization
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Title Multiresolution Imaging Using Bioluminescence Resonance Energy Transfer Identifies Distinct Biodistribution Profiles of Extracellular Vesicles and Exomeres with Redirected Tropism
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fadvs.202001467
https://www.ncbi.nlm.nih.gov/pubmed/33042758
https://www.proquest.com/docview/2448798813
https://www.proquest.com/docview/2648815544
https://www.proquest.com/docview/2450012191
https://pubmed.ncbi.nlm.nih.gov/PMC7539214
https://doaj.org/article/507974afa10f4003ae2bcbf96bda1580
Volume 7
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