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Single-nuclei isoform RNA sequencing unlocks barcoded exon connectivity in frozen brain tissue
Open accessAbstract
Single-nuclei RNA sequencing characterizes cell types at the gene level. However, compared to single-cell approaches, many single-nuclei cDNAs are purely intronic, lack barcodes and hinder the study of isoforms. Here we present single-nuclei isoform RNA sequencing (SnISOr-Seq). Using microfluidics, PCR-based artifact removal, target enrichment and long-read sequencing, SnISOr-Seq increased barcoded, exon-spanning long reads 7.5-fold compared to naive long-read single-nuclei sequencing. We applied SnISOr-Seq to adult human frontal cortex and found that exons associated with autism exhibit coordinated and highly cell-type-specific inclusion. We found two distinct combination patterns: those distinguishing neural cell types, enriched in TSS-exon, exon-polyadenylation-site and non-adjacent exon pairs, and those with multiple configurations within one cell type, enriched in adjacent exon pairs. Finally, we observed that human-specific exons are almost as tightly coordinated as conserved exons, implying that coordination can be rapidly established during evolution. SnISOr-Seq enables cell-type-specific long-read isoform analysis in human brain and in any frozen or hard-to-dissociate sample.
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“Emerging long-read sequencing approaches enable us to profile cellular transcriptomes at isoform resolution,8,31,32,33 thus providing new opportunities to model the relationships between isoforms using co-expression network analysis.”
From hdWGCNA identifies co-expression networks in high-dimensional transcriptomics data (2023) · cites this paper as [33]
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Metadata
- Authors
- Hardwick, S. A., Hu, W., Joglekar, A., Fan, L., Collier, P. G., Foord, C., Balacco, J., Lanjewar, S., Sampson, M. M., Koopmans, F., Prjibelski, A. D., Mikheenko, A., Belchikov, N., Jarroux, J., Lucas, A. B., Palkovits, M., Luo, W., Milner, T. A., Ndhlovu, L. C., Smit, A. B., Trojanowski, J. Q., Lee, V. M. Y., Fedrigo, O., Sloan, S. A., Tombácz, D., Ross, M. E., Jarvis, E., Boldogkői, Z., Gan, L., & Tilgner, H. U.
- Affiliations
- Weill Cornell Medicine (US)
- Rockefeller University (US)
- Emory University (US)
- Amsterdam Neuroscience (NL)
- St Petersburg University (RU)
- Agilent Technologies (United States) (US)
- Semmelweis University (HU)
- University of Pennsylvania (US)
- University of Szeged (HU)
- Corresponding author
- Tilgner, Hagen U.
- ORCID
- Hardwick, Simon A.
- Hu, Wen
- Joglekar, Anoushka
- Fan, Li
- Foord, Careen
- Balacco, Jennifer
- Lanjewar, Samantha
- Sampson, Maureen McGuirk
- Koopmans, Frank
- Prjibelski, Andrey D.
- Mikheenko, Alla
- Belchikov, Natan
- Jarroux, Julien
- Palkovits, Miklós
- Luo, Wenjie
- Milner, Teresa A.
- Ndhlovu, Lishomwa C.
- Smit, August B.
- Trojanowski, John Q.
- Lee, Virginia M. Y.
- Fedrigo, Olivier
- Sloan, Steven A.
- Tombácz, Dóra
- Ross, M. Elizabeth
- Jarvis, Erich
- Boldogkői, Zsolt
- Gan, Li
- Tilgner, Hagen U.
- Venue
- Nature Biotechnology
- Published
- 2022-03-07
- Volume
- 40
- Issue
- 7
- Pages
- 1082-1092
- ISSN
- 0733-222X (ISSN-L)
- 1087-0156
- 1546-1696
- PMC
- PMC9287170
- OpenAlex
- W4220958064
- Cited by
- 119
- References
- 59
- Citations by year
- 2026: 18 · 2025: 32 · 2024: 32 · 2023: 26 · 2022: 11
- FWCI
- 8.41
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature Biotechnology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- VU Research Portal (publishedVersion, other-oa)
- SZTE Publicatio Repozitórium (University of Szeged) (acceptedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Department of Health | National Health and Medical Research Council (APP1156531)
- Saint Petersburg State University (PURE 73023672)
- Semmelweis Egyetem (2017-1.2.1-NKP-2017-00002)
- Hungarian Brain Research Program, The Human Brain Tissue Bank, Semmelweis University
- U.S. Department of Health & Human Services | NIH | National Institute on Drug Abuse (DA08259, U01 DA53625, U01 DA053625-01)
- U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (HL136520)
- U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (UM1AI164599)
- U.S. Department of Health & Human Services | National Institutes of Health (U19 AG062418, R01AG051390, U54NS100717, R01AG054214)
- Howard Hughes Medical Institute
- U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (R01MH125956, 1RF1MH121267-01)
- Brain and Behavior Research Foundation (28172)
- Nemzeti Kutatási, Fejlesztési és Innovációs Hivatal (FK128252, K128247)
- U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (1R01NS105477, U54NS11717)
- U.S. Department of Health & Human Services | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD067244)
- Feil Family Foundation
- JPB Foundation
- U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (1R01GM135247-01)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- alternative splicing, barcoding, frozen brain tissue, human frontal cortex, autism spectrum disorder, long-read sequencing, microfluidics, target enrichment
- MeSH terms
- Brain, Exons, Humans, RNA, Alternative Splicing, Sequence Analysis, RNA, Protein Isoforms
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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