Atlas of Subcellular RNA Localization Revealed by APEX-Seq

We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales produced a nanometer-resolution spatial map of the human transcriptome as a resource, revealing extensive patterns of localiza...

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Published in	Cell Vol. 178; no. 2; pp. 473 - 490.e26
Main Authors	Fazal, Furqan M., Han, Shuo, Parker, Kevin R., Kaewsapsak, Pornchai, Xu, Jin, Boettiger, Alistair N., Chang, Howard Y., Ting, Alice Y.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 11.07.2019
Subjects	cycloheximide DNA-(Apurinic or Apyrimidinic Site) Lyase - metabolism Endonucleases - metabolism Fluorescent Dyes - chemistry HEK293 Cells Humans LADs messenger RNA Microscopy, Fluorescence mitochondria Mitochondria - genetics motifs Multifunctional Enzymes - metabolism nocodazole nuclear pore OXPHOS peroxidase retrotransposons RNA - chemistry RNA - metabolism RNA, Messenger - chemistry RNA, Messenger - metabolism sequence analysis Sequence Analysis, RNA - methods spatial transcriptomics Transcriptome translation UTRs cycloheximide spatial transcriptomics motifs UTRs LADs translation OXPHOS retrotransposons nocodazole
Online Access	Get full text
ISSN	0092-8674 1097-4172 1097-4172
DOI	10.1016/j.cell.2019.05.027

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Abstract	We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales produced a nanometer-resolution spatial map of the human transcriptome as a resource, revealing extensive patterns of localization for diverse RNA classes and transcript isoforms. We uncover a radial organization of the nuclear transcriptome, which is gated at the inner surface of the nuclear pore for cytoplasmic export of processed transcripts. We identify two distinct pathways of messenger RNA localization to mitochondria, each associated with specific sets of transcripts for building complementary macromolecular machines within the organelle. APEX-seq should be widely applicable to many systems, enabling comprehensive investigations of the spatial transcriptome. [Display omitted] •A transcriptome-wide subcellular RNA atlas was generated by proximity labeling•Isoform-level subcellular localization patterns for over 3,200 genes identified•RNA-transcript location correlates with genome architecture and protein localization•Two modes of mRNA localization to the outer mitochondrial membrane uncovered A newly developed technique reveals the subcellular transcriptomes at many landmarks in the nucleus and cytosol and connects mRNA localization to genome architecture, protein location, and local-translation mechanisms.
AbstractList	We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales produced a nanometer-resolution spatial map of the human transcriptome as a resource, revealing extensive patterns of localization for diverse RNA classes and transcript isoforms. We uncover a radial organization of the nuclear transcriptome, which is gated at the inner surface of the nuclear pore for cytoplasmic export of processed transcripts. We identify two distinct pathways of messenger RNA localization to mitochondria, each associated with specific sets of transcripts for building complementary macromolecular machines within the organelle. APEX-seq should be widely applicable to many systems, enabling comprehensive investigations of the spatial transcriptome. We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales produced a nanometer-resolution spatial map of the human transcriptome as a resource, revealing extensive patterns of localization for diverse RNA classes and transcript isoforms. We uncover a radial organization of the nuclear transcriptome, which is gated at the inner surface of the nuclear pore for cytoplasmic export of processed transcripts. We identify two distinct pathways of messenger RNA localization to mitochondria, each associated with specific sets of transcripts for building complementary macromolecular machines within the organelle. APEX-seq should be widely applicable to many systems, enabling comprehensive investigations of the spatial transcriptome. [Display omitted] •A transcriptome-wide subcellular RNA atlas was generated by proximity labeling•Isoform-level subcellular localization patterns for over 3,200 genes identified•RNA-transcript location correlates with genome architecture and protein localization•Two modes of mRNA localization to the outer mitochondrial membrane uncovered A newly developed technique reveals the subcellular transcriptomes at many landmarks in the nucleus and cytosol and connects mRNA localization to genome architecture, protein location, and local-translation mechanisms. We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales produced a nanometer-resolution spatial map of the human transcriptome as a resource, revealing extensive patterns of localization for diverse RNA classes and transcript isoforms. We uncover a radial organization of the nuclear transcriptome, which is gated at the inner surface of the nuclear pore for cytoplasmic export of processed transcripts. We identify two distinct pathways of messenger RNA localization to mitochondria, each associated with specific sets of transcripts for building complementary macromolecular machines within the organelle. APEX-seq should be widely applicable to many systems, enabling comprehensive investigations of the spatial transcriptome. A newly-developed technique reveals the subcellular transcriptomes at many landmarks in the nucleus and cytosol, and connects mRNA localization to genome architecture, protein location and local-translation mechanisms. We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales produced a nanometer-resolution spatial map of the human transcriptome as a resource, revealing extensive patterns of localization for diverse RNA classes and transcript isoforms. We uncover a radial organization of the nuclear transcriptome, which is gated at the inner surface of the nuclear pore for cytoplasmic export of processed transcripts. We identify two distinct pathways of messenger RNA localization to mitochondria, each associated with specific sets of transcripts for building complementary macromolecular machines within the organelle. APEX-seq should be widely applicable to many systems, enabling comprehensive investigations of the spatial transcriptome. We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales produced a nanometer-resolution spatial map of the human transcriptome as a resource, revealing extensive patterns of localization for diverse RNA classes and transcript isoforms. We uncover a radial organization of the nuclear transcriptome, which is gated at the inner surface of the nuclear pore for cytoplasmic export of processed transcripts. We identify two distinct pathways of messenger RNA localization to mitochondria, each associated with specific sets of transcripts for building complementary macromolecular machines within the organelle. APEX-seq should be widely applicable to many systems, enabling comprehensive investigations of the spatial transcriptome.We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct subcellular locales produced a nanometer-resolution spatial map of the human transcriptome as a resource, revealing extensive patterns of localization for diverse RNA classes and transcript isoforms. We uncover a radial organization of the nuclear transcriptome, which is gated at the inner surface of the nuclear pore for cytoplasmic export of processed transcripts. We identify two distinct pathways of messenger RNA localization to mitochondria, each associated with specific sets of transcripts for building complementary macromolecular machines within the organelle. APEX-seq should be widely applicable to many systems, enabling comprehensive investigations of the spatial transcriptome.
Author	Ting, Alice Y. Boettiger, Alistair N. Han, Shuo Fazal, Furqan M. Chang, Howard Y. Parker, Kevin R. Xu, Jin Kaewsapsak, Pornchai
AuthorAffiliation	2 Department of Dermatology, Stanford University School of Medicine, Stanford, CA 94305, USA 9 These authors contributed equally 1 Center for Personal Dynamics Regulomes, Stanford University School of Medicine, Stanford, CA 94305, USA 4 Department of Chemistry, Stanford University, Stanford, CA 94305, USA 7 Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA 94305, USA 8 Chan Zuckerberg Biohub, San Francisco, CA 94158, USA 6 Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA 10 These authors contributed equally 5 Department of Biology, Stanford University, Stanford, CA 94305, USA 11 Lead contact 3 Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA
AuthorAffiliation_xml	– name: 1 Center for Personal Dynamics Regulomes, Stanford University School of Medicine, Stanford, CA 94305, USA – name: 2 Department of Dermatology, Stanford University School of Medicine, Stanford, CA 94305, USA – name: 9 These authors contributed equally – name: 11 Lead contact – name: 4 Department of Chemistry, Stanford University, Stanford, CA 94305, USA – name: 5 Department of Biology, Stanford University, Stanford, CA 94305, USA – name: 6 Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA – name: 8 Chan Zuckerberg Biohub, San Francisco, CA 94158, USA – name: 3 Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA – name: 10 These authors contributed equally – name: 7 Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA 94305, USA
Author_xml	– sequence: 1 givenname: Furqan M. surname: Fazal fullname: Fazal, Furqan M. organization: Center for Personal Dynamics Regulomes, Stanford University School of Medicine, Stanford, CA 94305, USA – sequence: 2 givenname: Shuo surname: Han fullname: Han, Shuo organization: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA – sequence: 3 givenname: Kevin R. surname: Parker fullname: Parker, Kevin R. organization: Center for Personal Dynamics Regulomes, Stanford University School of Medicine, Stanford, CA 94305, USA – sequence: 4 givenname: Pornchai surname: Kaewsapsak fullname: Kaewsapsak, Pornchai organization: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA – sequence: 5 givenname: Jin surname: Xu fullname: Xu, Jin organization: Center for Personal Dynamics Regulomes, Stanford University School of Medicine, Stanford, CA 94305, USA – sequence: 6 givenname: Alistair N. surname: Boettiger fullname: Boettiger, Alistair N. organization: Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA – sequence: 7 givenname: Howard Y. surname: Chang fullname: Chang, Howard Y. email: howchang@stanford.edu organization: Center for Personal Dynamics Regulomes, Stanford University School of Medicine, Stanford, CA 94305, USA – sequence: 8 givenname: Alice Y. surname: Ting fullname: Ting, Alice Y. email: ayting@stanford.edu organization: Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31230715$$D View this record in MEDLINE/PubMed
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Copyright	2019 Elsevier Inc. Copyright © 2019 Elsevier Inc. All rights reserved.
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Keywords	cycloheximide spatial transcriptomics motifs UTRs LADs translation OXPHOS retrotransposons nocodazole
Language	English
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS F.M.F., P.K., H.Y.C and A.Y.T. conceived the project. F.M.F., S.H., P.K., H.Y.C. and A.Y.T. designed experiments. F.M.F., S.H. and P.K. performed all experiments, unless otherwise noted. F.M.F. designed and carried out sequencing experiments. S.H., A.N.B. and A.Y.T. designed and carried out sequential FISH experiments. F.M.F, S.H, K.R.P., P.K, J.X. and A.Y.T. analyzed data. F.M.F., S.H., H.Y.C. and A.Y.T. wrote the paper with input from all authors. H.Y.C. and A.Y.T. jointly supervised work and acquired funding.
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Snippet	We introduce APEX-seq, a method for RNA sequencing based on direct proximity labeling of RNA using the peroxidase enzyme APEX2. APEX-seq in nine distinct...
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SubjectTerms	cycloheximide DNA-(Apurinic or Apyrimidinic Site) Lyase - metabolism Endonucleases - metabolism Fluorescent Dyes - chemistry HEK293 Cells Humans LADs messenger RNA Microscopy, Fluorescence mitochondria Mitochondria - genetics motifs Multifunctional Enzymes - metabolism nocodazole nuclear pore OXPHOS peroxidase retrotransposons RNA - chemistry RNA - metabolism RNA, Messenger - chemistry RNA, Messenger - metabolism sequence analysis Sequence Analysis, RNA - methods spatial transcriptomics Transcriptome translation UTRs
Title	Atlas of Subcellular RNA Localization Revealed by APEX-Seq
URI	https://dx.doi.org/10.1016/j.cell.2019.05.027 https://www.ncbi.nlm.nih.gov/pubmed/31230715 https://www.proquest.com/docview/2246243398 https://www.proquest.com/docview/2305173387 https://pubmed.ncbi.nlm.nih.gov/PMC6786773
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