Dense, continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissues

Abstract Lipid membranes are key to the nanoscale compartmentalization of biological systems, but fluorescent visualization of them in intact tissues, with nanoscale precision, is challenging to do with high labeling density. Here, we report ultrastructural membrane expansion microscopy (umExM), whi...

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Main Authors: Tay Won Shin, Hao Wang, Chi Zhang, Bobae An, Yangning Lu, Elizabeth Zhang, Xiaotang Lu, Emmanouil D. Karagiannis, Jeong Seuk Kang, Amauche Emenari, Panagiotis Symvoulidis, Shoh Asano, Leanne Lin, Emma K. Costa, IMAXT Grand Challenge Consortium, Adam H. Marblestone, Narayanan Kasthuri, Li-Huei Tsai, Edward S. Boyden
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-56641-z
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author Tay Won Shin
Hao Wang
Chi Zhang
Bobae An
Yangning Lu
Elizabeth Zhang
Xiaotang Lu
Emmanouil D. Karagiannis
Jeong Seuk Kang
Amauche Emenari
Panagiotis Symvoulidis
Shoh Asano
Leanne Lin
Emma K. Costa
IMAXT Grand Challenge Consortium
Adam H. Marblestone
Narayanan Kasthuri
Li-Huei Tsai
Edward S. Boyden
author_facet Tay Won Shin
Hao Wang
Chi Zhang
Bobae An
Yangning Lu
Elizabeth Zhang
Xiaotang Lu
Emmanouil D. Karagiannis
Jeong Seuk Kang
Amauche Emenari
Panagiotis Symvoulidis
Shoh Asano
Leanne Lin
Emma K. Costa
IMAXT Grand Challenge Consortium
Adam H. Marblestone
Narayanan Kasthuri
Li-Huei Tsai
Edward S. Boyden
author_sort Tay Won Shin
collection DOAJ
description Abstract Lipid membranes are key to the nanoscale compartmentalization of biological systems, but fluorescent visualization of them in intact tissues, with nanoscale precision, is challenging to do with high labeling density. Here, we report ultrastructural membrane expansion microscopy (umExM), which combines an innovative membrane label and optimized expansion microscopy protocol, to support dense labeling of membranes in tissues for nanoscale visualization. We validate the high signal-to-background ratio, and uniformity and continuity, of umExM membrane labeling in brain slices, which supports the imaging of membranes and proteins at a resolution of ~60 nm on a confocal microscope. We demonstrate the utility of umExM for the segmentation and tracing of neuronal processes, such as axons, in mouse brain tissue. Combining umExM with optical fluctuation imaging, or iterating the expansion process, yields ~35 nm resolution imaging, pointing towards the potential for electron microscopy resolution visualization of brain membranes on ordinary light microscopes.
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spelling doaj-art-670f2abb61e14bc2863da95da7a74b582025-08-20T03:00:58ZengNature PortfolioNature Communications2041-17232025-02-0116111710.1038/s41467-025-56641-zDense, continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissuesTay Won Shin0Hao Wang1Chi Zhang2Bobae An3Yangning Lu4Elizabeth Zhang5Xiaotang Lu6Emmanouil D. Karagiannis7Jeong Seuk Kang8Amauche Emenari9Panagiotis Symvoulidis10Shoh Asano11Leanne Lin12Emma K. Costa13IMAXT Grand Challenge ConsortiumAdam H. Marblestone14Narayanan Kasthuri15Li-Huei Tsai16Edward S. Boyden17McGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyDepartment of Cellular and Molecular Biology, Harvard UniversityMcGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyDepartment of Biological Engineering, Massachusetts Institute of TechnologyDepartment of Brain and Cognitive Sciences, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyCenter for Nanoscale Materials, Argonne National LaboratoryDepartment of Brain and Cognitive Sciences, Massachusetts Institute of TechnologyMcGovern Institute, Massachusetts Institute of TechnologyAbstract Lipid membranes are key to the nanoscale compartmentalization of biological systems, but fluorescent visualization of them in intact tissues, with nanoscale precision, is challenging to do with high labeling density. Here, we report ultrastructural membrane expansion microscopy (umExM), which combines an innovative membrane label and optimized expansion microscopy protocol, to support dense labeling of membranes in tissues for nanoscale visualization. We validate the high signal-to-background ratio, and uniformity and continuity, of umExM membrane labeling in brain slices, which supports the imaging of membranes and proteins at a resolution of ~60 nm on a confocal microscope. We demonstrate the utility of umExM for the segmentation and tracing of neuronal processes, such as axons, in mouse brain tissue. Combining umExM with optical fluctuation imaging, or iterating the expansion process, yields ~35 nm resolution imaging, pointing towards the potential for electron microscopy resolution visualization of brain membranes on ordinary light microscopes.https://doi.org/10.1038/s41467-025-56641-z
spellingShingle Tay Won Shin
Hao Wang
Chi Zhang
Bobae An
Yangning Lu
Elizabeth Zhang
Xiaotang Lu
Emmanouil D. Karagiannis
Jeong Seuk Kang
Amauche Emenari
Panagiotis Symvoulidis
Shoh Asano
Leanne Lin
Emma K. Costa
IMAXT Grand Challenge Consortium
Adam H. Marblestone
Narayanan Kasthuri
Li-Huei Tsai
Edward S. Boyden
Dense, continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissues
Nature Communications
title Dense, continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissues
title_full Dense, continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissues
title_fullStr Dense, continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissues
title_full_unstemmed Dense, continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissues
title_short Dense, continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissues
title_sort dense continuous membrane labeling and expansion microscopy visualization of ultrastructure in tissues
url https://doi.org/10.1038/s41467-025-56641-z
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