Unraveling cellular complexity with transient adapters in highly multiplexed super-resolution imaging

Mapping the intricate spatial relationships between the many different molecules inside a cell is essential to understanding cellular functions in all their complexity. Super-resolution fluorescence microscopy offers the required spatial resolution but struggles to reveal more than four different ta...

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Published inCell Vol. 187; no. 7; pp. 1769 - 1784.e18
Main Authors Schueder, Florian, Rivera-Molina, Felix, Su, Maohan, Marin, Zach, Kidd, Phylicia, Rothman, James E., Toomre, Derek, Bewersdorf, Joerg
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 28.03.2024
Subjects
Animals
DNA
DNA-PAINT
FLASH-PAINT
fluorescence microscopy
Golgi Apparatus
Mammals
Microscopy, Fluorescence - methods
multiplexing
nanoscopy
Oligonucleotides
Proteins
spatial omics
super-resolution
nanoscopy
FLASH-PAINT
multiplexing
spatial omics
DNA-PAINT
super-resolution
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Abstract Mapping the intricate spatial relationships between the many different molecules inside a cell is essential to understanding cellular functions in all their complexity. Super-resolution fluorescence microscopy offers the required spatial resolution but struggles to reveal more than four different targets simultaneously. Exchanging labels in subsequent imaging rounds for multiplexed imaging extends this number but is limited by its low throughput. Here, we present a method for rapid multiplexed super-resolution microscopy that can, in principle, be applied to a nearly unlimited number of molecular targets by leveraging fluorogenic labeling in conjunction with transient adapter-mediated switching for high-throughput DNA-PAINT (FLASH-PAINT). We demonstrate the versatility of FLASH-PAINT with four applications: mapping nine proteins in a single mammalian cell, elucidating the functional organization of primary cilia by nine-target imaging, revealing the changes in proximity of thirteen different targets in unperturbed and dissociated Golgi stacks, and investigating and quantifying inter-organelle contacts at 3D super-resolution. [Display omitted] •FLASH-PAINT enables highly multiplexed super-resolution imaging•Transient adapters and erasers allow for fast, efficient, and gentle label exchange•Multiplexed super-resolution imaging reveals complex cilia and Golgi organization•3D FLASH-PAINT allows for quantification of organelle contact site numbers and areas Development of FLASH-PAINT enables rapid and efficient visualization of cellular organelles, using a potentially unlimited number of labels.
AbstractList Mapping the intricate spatial relationships between the many different molecules inside a cell is essential to understanding cellular functions in all their complexity. Super-resolution fluorescence microscopy offers the required spatial resolution but struggles to reveal more than four different targets simultaneously. Exchanging labels in subsequent imaging rounds for multiplexed imaging extends this number but is limited by its low throughput. Here, we present a method for rapid multiplexed super-resolution microscopy that can, in principle, be applied to a nearly unlimited number of molecular targets by leveraging fluorogenic labeling in conjunction with transient adapter-mediated switching for high-throughput DNA-PAINT (FLASH-PAINT). We demonstrate the versatility of FLASH-PAINT with four applications: mapping nine proteins in a single mammalian cell, elucidating the functional organization of primary cilia by nine-target imaging, revealing the changes in proximity of thirteen different targets in unperturbed and dissociated Golgi stacks, and investigating and quantifying inter-organelle contacts at 3D super-resolution. [Display omitted] •FLASH-PAINT enables highly multiplexed super-resolution imaging•Transient adapters and erasers allow for fast, efficient, and gentle label exchange•Multiplexed super-resolution imaging reveals complex cilia and Golgi organization•3D FLASH-PAINT allows for quantification of organelle contact site numbers and areas Development of FLASH-PAINT enables rapid and efficient visualization of cellular organelles, using a potentially unlimited number of labels.
Mapping the intricate spatial relationships between the many different molecules inside a cell is essential to understanding cellular functions in all their complexity. Super-resolution fluorescence microscopy offers the required spatial resolution but struggles to reveal more than four different targets simultaneously. Exchanging labels in subsequent imaging rounds for multiplexed imaging extends this number but is limited by its low throughput. Here we present a method for rapid multiplexed super-resolution microscopy that can, in principle, be applied to a nearly unlimited number of molecular targets by leveraging fluorogenic labeling in conjunction with Transient Adapter-mediated switching for high-throughput DNA-PAINT (FLASH-PAINT). We demonstrate the versatility of FLASH-PAINT with four applications: mapping nine proteins in a single mammalian cell, elucidating the functional organization of primary cilia by nine-target imaging, revealing the changes in proximity of thirteen different targets in unperturbed and dissociated Golgi stacks, and investigating and quantifying inter-organelle contacts at 3D super- resolution.
Mapping the intricate spatial relationships between the many different molecules inside a cell is essential to understanding cellular functions in all their complexity. Super-resolution fluorescence microscopy offers the required spatial resolution but struggles to reveal more than four different targets simultaneously. Exchanging labels in subsequent imaging rounds for multiplexed imaging extends this number but is limited by its low throughput. Here, we present a method for rapid multiplexed super-resolution microscopy that can, in principle, be applied to a nearly unlimited number of molecular targets by leveraging fluorogenic labeling in conjunction with transient adapter-mediated switching for high-throughput DNA-PAINT (FLASH-PAINT). We demonstrate the versatility of FLASH-PAINT with four applications: mapping nine proteins in a single mammalian cell, elucidating the functional organization of primary cilia by nine-target imaging, revealing the changes in proximity of thirteen different targets in unperturbed and dissociated Golgi stacks, and investigating and quantifying inter-organelle contacts at 3D super-resolution.Mapping the intricate spatial relationships between the many different molecules inside a cell is essential to understanding cellular functions in all their complexity. Super-resolution fluorescence microscopy offers the required spatial resolution but struggles to reveal more than four different targets simultaneously. Exchanging labels in subsequent imaging rounds for multiplexed imaging extends this number but is limited by its low throughput. Here, we present a method for rapid multiplexed super-resolution microscopy that can, in principle, be applied to a nearly unlimited number of molecular targets by leveraging fluorogenic labeling in conjunction with transient adapter-mediated switching for high-throughput DNA-PAINT (FLASH-PAINT). We demonstrate the versatility of FLASH-PAINT with four applications: mapping nine proteins in a single mammalian cell, elucidating the functional organization of primary cilia by nine-target imaging, revealing the changes in proximity of thirteen different targets in unperturbed and dissociated Golgi stacks, and investigating and quantifying inter-organelle contacts at 3D super-resolution.
Author Bewersdorf, Joerg
Su, Maohan
Marin, Zach
Rothman, James E.
Rivera-Molina, Felix
Toomre, Derek
Schueder, Florian
Kidd, Phylicia
AuthorAffiliation 5 Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA
3 Department of Biomedical Engineering, Yale University, New Haven, CT, USA
4 Nanobiology Institute, Yale University, West Haven, CT, USA
2 Department of Microbial Pathogenesis, Yale School of Medicine, New Haven, CT, USA
6 Department of Physics, Yale University, New Haven, CT, USA
1 Department of Cell Biology, Yale School of Medicine, New Haven, CT, USA
7 Lead contact
AuthorAffiliation_xml – name: 1 Department of Cell Biology, Yale School of Medicine, New Haven, CT, USA
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Keywords nanoscopy
FLASH-PAINT
multiplexing
spatial omics
DNA-PAINT
super-resolution
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content type line 23
F.S. and J.B. conceived and designed the study. F.S. performed all experiments except the cilia experiments. F.R.-M. performed the cilia experiments. F.S. and F.R.-M. analyzed the cilia data. P.K. contributed to the design of the 9-plexed experiment. M.S. and F.S. designed, performed, and analyzed the Golgi experiment. F.S. and Z.M. designed and performed the ROI-based abundance analysis and UMAP analysis of the Golgi data. F.S. and J.B. wrote the manuscript with input from all authors. D.K.T. and J.E.R. supervised parts of the study. J.B supervised the study.
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Snippet Mapping the intricate spatial relationships between the many different molecules inside a cell is essential to understanding cellular functions in all their...
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SubjectTerms Animals
DNA
DNA-PAINT
FLASH-PAINT
fluorescence microscopy
Golgi Apparatus
Mammals
Microscopy, Fluorescence - methods
multiplexing
nanoscopy
Oligonucleotides
Proteins
spatial omics
super-resolution
Title Unraveling cellular complexity with transient adapters in highly multiplexed super-resolution imaging
URI https://dx.doi.org/10.1016/j.cell.2024.02.033
https://www.ncbi.nlm.nih.gov/pubmed/38552613
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https://pubmed.ncbi.nlm.nih.gov/PMC12135969
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