Multi-resolution imaging using bioluminescence resonance energy transfer identifies distinct biodistribution profiles of extracellular vesicles and exomeres with redirected tropism
Extracellular particles (EP) including extracellular vesicles (EVs) and exomeres have been shown to 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. We ther...
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| Published in | bioRxiv |
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| Main Authors | , , , , , , , , , , , , , , , , , , |
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| Language | English |
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Cold Spring Harbor Laboratory
09.07.2020
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| Edition | 1.2 |
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| Abstract | Extracellular particles (EP) including extracellular vesicles (EVs) and exomeres have been shown to 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. We therefore created a bioluminescence resonance energy transfer (BRET)-based reporter, PalmGRET, to enable pan-EP labelling 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, we show that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. We further demonstrate that gene knockdown of lung-tropic membrane proteins, solute carrier organic anion transporter family member 2A1 (Slco2a1), alanine aminopeptidase (Cd13) and chloride intracellular channel (Clic1) decreases HCC-EP distribution to the lungs and yields distinct biodistribution profiles. We anticipate that EP-specific imaging, quantitative assays and detailed in vivo characterization to be a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design. |
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| AbstractList | Extracellular particles (EP) including extracellular vesicles (EVs) and exomeres have been shown to 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. We therefore created a bioluminescence resonance energy transfer (BRET)-based reporter, PalmGRET, to enable pan-EP labelling 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, we show that EPs released by lung metastatic hepatocellular carcinoma (HCC) exhibit lung tropism with varying distributions to other major organs in immunocompetent mice. We further demonstrate that gene knockdown of lung-tropic membrane proteins, solute carrier organic anion transporter family member 2A1 (Slco2a1), alanine aminopeptidase (Cd13) and chloride intracellular channel (Clic1) decreases HCC-EP distribution to the lungs and yields distinct biodistribution profiles. We anticipate that EP-specific imaging, quantitative assays and detailed in vivo characterization to be a starting point for more accurate and comprehensive in vivo models of EP biology and therapeutic design. |
| Author | Chen, Yunching Wu, Anthony Yan-Tang Yang, Alan Ling Huang, Hsi-Chien Wu, Syuan Juan, Hsueh-Fen Ericsson, Maria Sung, Yun-Chieh Guo, Vanessa Ho, Meng-Ru Chou, Steven Ting-Yu Chuang, Ju-Chen Ueda, Koji Chien, Jasper Che-Yung Lai, Charles Pin-Kuang Cheung, Chantal Hoi Yin Ko, John Jun-Sheng Chen, Yen-Ju Lin, Wan-Wan |
| Author_xml | – sequence: 1 givenname: Anthony Yan-Tang surname: Wu fullname: Wu, Anthony Yan-Tang organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 2 givenname: Yun-Chieh surname: Sung fullname: Sung, Yun-Chieh organization: Department of Chemical Engineering, National Tsing Hua University 30013 – sequence: 3 givenname: Yen-Ju surname: Chen fullname: Chen, Yen-Ju organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 4 givenname: Steven Ting-Yu surname: Chou fullname: Chou, Steven Ting-Yu organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 5 givenname: Vanessa surname: Guo fullname: Guo, Vanessa organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 6 givenname: Jasper Che-Yung surname: Chien fullname: Chien, Jasper Che-Yung organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 7 givenname: John Jun-Sheng surname: Ko fullname: Ko, John Jun-Sheng organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 8 givenname: Alan Ling surname: Yang fullname: Yang, Alan Ling organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 9 givenname: Hsi-Chien surname: Huang fullname: Huang, Hsi-Chien organization: Department of Chemical Engineering, National Tsing Hua University 30013 – sequence: 10 givenname: Ju-Chen surname: Chuang fullname: Chuang, Ju-Chen organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 11 givenname: Syuan surname: Wu fullname: Wu, Syuan organization: Institute of Atomic and Molecular Sciences, Academia Sinica – sequence: 12 givenname: Meng-Ru surname: Ho fullname: Ho, Meng-Ru organization: Institute of Biological Chemistry, Academia Sinica – sequence: 13 givenname: Maria surname: Ericsson fullname: Ericsson, Maria organization: Department of Cell Biology, Harvard Medical School – sequence: 14 givenname: Wan-Wan surname: Lin fullname: Lin, Wan-Wan organization: Department of Pharmacology, College of Medicine, National Taiwan University – sequence: 15 givenname: Chantal Hoi Yin surname: Cheung fullname: Cheung, Chantal Hoi Yin organization: Department of Life Science, National Taiwan University – sequence: 16 givenname: Hsueh-Fen surname: Juan fullname: Juan, Hsueh-Fen organization: Department of Life Science, National Taiwan University – sequence: 17 givenname: Koji surname: Ueda fullname: Ueda, Koji organization: Cancer Proteomics Group, Cancer Precision Medicine Center, Japanese Foundation for Cancer Research – sequence: 18 givenname: Yunching surname: Chen fullname: Chen, Yunching organization: Institute of Biomedical Engineering and Frontier Research Center on Fundamental and Applied Sciences of Matters, National Tsing Hua University – sequence: 19 givenname: Charles Pin-Kuang surname: Lai fullname: Lai, Charles Pin-Kuang email: laicharles@sinica.edu.tw organization: Genome and Systems Biology Degree Program, National Taiwan University and Academia Sinica |
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| ContentType | Paper |
| Copyright | 2020, Posted by Cold Spring Harbor Laboratory |
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| DOI | 10.1101/2020.03.27.012625 |
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| Keywords | exomeres biodistribution bioluminescence resonance energy transfer extracellular particles exosomes Extracellular vesicles microvesicles redirected tropism |
| Language | English |
| License | This pre-print is available under a Creative Commons License (Attribution-NonCommercial-NoDerivs 4.0 International), CC BY-NC-ND 4.0, as described at http://creativecommons.org/licenses/by-nc-nd/4.0 |
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| Notes | Competing Interest Statement: The authors have declared no competing interest. |
| OpenAccessLink | https://www.biorxiv.org/content/10.1101/2020.03.27.012625 |
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| Snippet | Extracellular particles (EP) including extracellular vesicles (EVs) and exomeres have been shown to play significant roles in diseases and therapeutic... |
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| Title | Multi-resolution imaging using bioluminescence resonance energy transfer identifies distinct biodistribution profiles of extracellular vesicles and exomeres with redirected tropism |
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