Non-coding deletions identify Maenli lncRNA as a limb-specific En1 regulator.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
04 2021
Historique:
received: 05 10 2019
accepted: 07 01 2021
pubmed: 12 2 2021
medline: 10 4 2021
entrez: 11 2 2021
Statut: ppublish

Résumé

Long non-coding RNAs (lncRNAs) can be important components in gene-regulatory networks

Identifiants

pubmed: 33568816
doi: 10.1038/s41586-021-03208-9
pii: 10.1038/s41586-021-03208-9
doi:

Substances chimiques

Chromatin 0
EN1 protein, human 0
Homeodomain Proteins 0
RNA, Long Noncoding 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

93-98

Subventions

Organisme : Wellcome Trust
ID : 206475/Z/17/Z
Pays : United Kingdom

Références

Kopp, F. & Mendell, J. T. Functional classification and experimental dissection of long noncoding RNAs. Cell 172, 393–407 (2018).
pubmed: 29373828 pmcid: 5978744
Hon, C. C. et al. An atlas of human long non-coding RNAs with accurate 5′ ends. Nature 543, 199–204 (2017).
pubmed: 28241135 pmcid: 6857182
Engreitz, J. M. et al. Local regulation of gene expression by lncRNA promoters, transcription and splicing. Nature 539, 452–455 (2016).
pubmed: 27783602 pmcid: 6853796
Loomis, C. A. et al. The mouse Engrailed-1 gene and ventral limb patterning. Nature 382, 360–363 (1996).
pubmed: 8684466
Wurst, W., Auerbach, A. B. & Joyner, A. L. Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120, 2065–2075 (1994).
pubmed: 7925010
Franke, M. et al. Formation of new chromatin domains determines pathogenicity of genomic duplications. Nature 538, 265–269 (2016).
pubmed: 27706140
Kragesteen, B. K. et al. Dynamic 3D chromatin architecture contributes to enhancer specificity and limb morphogenesis. Nat. Genet. 50, 1463–1473 (2018).
pubmed: 30262816
Huettl, R. E. et al. Engrailed 1 mediates correct formation of limb innervation through two distinct mechanisms. PLoS ONE 10, e0118505 (2015).
pubmed: 25710467 pmcid: 4340014
Andrey, G. et al. Characterization of hundreds of regulatory landscapes in developing limbs reveals two regimes of chromatin folding. Genome Res. 27, 223–233 (2017).
doi: 10.1101/gr.213066.116 pubmed: 27923844 pmcid: 5287228
Xiang, J. F. et al. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res. 24, 513–531 (2014).
pubmed: 24662484 pmcid: 4011346
Cho, S. W. et al. Promoter of lncRNA gene PVT1 Is a tumor-suppressor DNA boundary element. Cell 173, 1398–1412 (2018).
pubmed: 29731168 pmcid: 5984165
Isoda, T. et al. Non-coding transcription instructs chromatin folding and compartmentalization to dictate enhancer-promoter communication and T cell fate. Cell 171, 103–119 (2017).
pubmed: 28938112 pmcid: 5621651
Vian, L. et al. The energetics and physiological impact of cohesin extrusion. Cell 175, 292–294 (2018).
pubmed: 30241609 pmcid: 6251724
Kraft, K. et al. Serial genomic inversions induce tissue-specific architectural stripes, gene misexpression and congenital malformations. Nat. Cell Biol. 21, 305–310 (2019).
pubmed: 30742094
Wang, K. C. et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120–124 (2011).
pubmed: 21423168 pmcid: 3670758
Gutschner, T. & Diederichs, S. The hallmarks of cancer: a long non-coding RNA point of view. RNA Biol. 9, 703–719 (2012).
pubmed: 22664915 pmcid: 3495743
Ishii, N. et al. Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. J. Hum. Genet. 51, 1087–1099 (2006).
pubmed: 17066261
Broadbent, H. M. et al. Susceptibility to coronary artery disease and diabetes is encoded by distinct, tightly linked SNPs in the ANRIL locus on chromosome 9p. Hum. Mol. Genet. 17, 806–814 (2008).
pubmed: 18048406
Cabianca, D. S. et al. A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149, 819–831 (2012).
pubmed: 22541069 pmcid: 3350859
van Dijk, M. et al. HELLP babies link a novel lincRNA to the trophoblast cell cycle. J. Clin. Invest. 122, 4003–4011 (2012).
pubmed: 23093777 pmcid: 3484460
Maass, P. G. et al. A misplaced lncRNA causes brachydactyly in humans. J. Clin. Invest. 122, 3990–4002 (2012).
pubmed: 23093776 pmcid: 3485082
Castellanos-Rubio, A. et al. A long noncoding RNA associated with susceptibility to celiac disease. Science 352, 91–95 (2016).
pubmed: 27034373 pmcid: 4994711
Royer-Bertrand, B. et al. Mutations in the heat-shock protein A9 (HSPA9) gene cause the EVEN-PLUS syndrome of congenital malformations and skeletal dysplasia. Sci. Rep. 5, 17154 (2015).
pubmed: 26598328 pmcid: 4657157
Van der Auwera, G. A. et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinformatics. 43, 11.10.1–11.10.33 (2013).
Karczewski, K. J. et al. The ExAC browser: displaying reference data information from over 60 000 exomes. Nucleic Acids Res. 45 (D1), D840–D845 (2017).
pubmed: 27899611
Lek, M. et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature 536, 285–291 (2016).
pubmed: 27535533 pmcid: 5018207
Auton, A. et al. A global reference for human genetic variation. Nature 526, 68–74 (2015).
pubmed: 26432245
Naslavsky, M. S. et al. Exomic variants of an elderly cohort of Brazilians in the ABraOM database. Hum. Mutat. 38, 751–763 (2017).
pubmed: 28332257
Kraft, K. et al. Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in mice. Cell Rep. 10, 833–839 (2015).
pubmed: 25660031
George, S. H. et al. Developmental and adult phenotyping directly from mutant embryonic stem cells. Proc. Natl Acad. Sci. USA 104, 4455–4460 (2007).
pubmed: 17360545 pmcid: 1838622
Artus, J. & Hadjantonakis, A. K. Generation of chimeras by aggregation of embryonic stem cells with diploid or tetraploid mouse embryos. Methods Mol. Biol. 693, 37–56 (2011).
pubmed: 21080273
Liska, F. et al. Impairment of Sox9 expression in limb buds of rats homozygous for hypodactyly mutation. Folia Biol. 56, 58–65 (2010).
Wingett, S. et al. HiCUP: pipeline for mapping and processing Hi-C data. F1000Res. 4, 1310 (2015).
pubmed: 26835000 pmcid: 4706059
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
doi: 10.1038/nmeth.1923 pubmed: 22388286 pmcid: 3322381
Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3, 95–98 (2016).
pubmed: 27467249 pmcid: 5846465
Rao, S. S. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014).
pubmed: 25497547 pmcid: 5635824
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
Lupiáñez, D. G. et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012–1025 (2015).
pubmed: 25959774 pmcid: 4791538
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281 pmcid: 4302049
Wolock, S. L., Lopez, R. & Klein, A. M. Scrublet: computational identification of cell doublets in single-cell transcriptomic data. Cell Syst. 8, 281–291 (2019).
pubmed: 30954476 pmcid: 6625319
Hafemeister, C. & Satija, R. Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression. Genome Biol. 20, 296 (2019).
pubmed: 31870423 pmcid: 6927181
Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018).
pubmed: 29608179 pmcid: 6700744
Ibrahim, D. M. et al. Distinct global shifts in genomic binding profiles of limb malformation-associated HOXD13 mutations. Genome Res. 23, 2091–2102 (2013).
pubmed: 23995701 pmcid: 3847778
Lee, T. I., Johnstone, S. E. & Young, R. A. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 1, 729–748 (2006).
pubmed: 17406303 pmcid: 3004291
Paliou, C. et al. Preformed chromatin topology assists transcriptional robustness of Shh during limb development. Proc. Natl Acad. Sci. USA 116, 12390–12399 (2019).
pubmed: 31147463 pmcid: 6589666
Ramírez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44 (W1), W160–W165 (2016).
pubmed: 27079975 pmcid: 4987876
Vogel, M. J., Peric-Hupkes, D. & van Steensel, B. Detection of in vivo protein-DNA interactions using DamID in mammalian cells. Nat. Protoc. 2, 1467–1478 (2007).
pubmed: 17545983
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234
Gagnon, K. T., Li, L., Janowski, B. A. & Corey, D. R. Analysis of nuclear RNA interference in human cells by subcellular fractionation and Argonaute loading. Nat. Protoc. 9, 2045–2060 (2014).
pubmed: 25079428 pmcid: 4251768
Grote, P. et al. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev. Cell 24, 206–214 (2013).
pubmed: 23369715 pmcid: 4149175
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2
pubmed: 11846609

Auteurs

Lila Allou (L)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.
Institute for Medical and Human Genetics, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Sara Balzano (S)

Medical Genetics Unit, Department of Computational Biology, University of Lausanne, Lausanne, Switzerland.
Division of Genetic Medicine, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Andreas Magg (A)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.
Institute for Medical and Human Genetics, Charité-Universitätsmedizin Berlin, Berlin, Germany.
Berlin-Brandenburg Center for Regenerative Therapies, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Mathieu Quinodoz (M)

Medical Genetics Unit, Department of Computational Biology, University of Lausanne, Lausanne, Switzerland.
Institute of Molecular and Clinical Ophthalmology Basel (IOB), Basel, Switzerland.
Department of Ophthalmology, University of Basel, Basel, Switzerland.

Beryl Royer-Bertrand (B)

Division of Genetic Medicine, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Robert Schöpflin (R)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.
Institute for Medical and Human Genetics, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Wing-Lee Chan (WL)

Institute for Medical and Human Genetics, Charité-Universitätsmedizin Berlin, Berlin, Germany.
Berlin-Brandenburg Center for Regenerative Therapies, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Carlos E Speck-Martins (CE)

Genetic Unit, SARAH Network of Rehabilitation Hospitals, Brasilia, Brazil.

Daniel Rocha Carvalho (DR)

Genetic Unit, SARAH Network of Rehabilitation Hospitals, Brasilia, Brazil.

Luciano Farage (L)

Instituto de Cardiologia do Distrito Federal, Brasilia, Brazil.

Charles Marques Lourenço (CM)

Faculdade de Medicina, Centro Universitario Estácio, Ribeirão Preto, Brazil.

Regina Albuquerque (R)

Faculdade Estadual de Medicina de São José do Rio Preto (FAMERP), São José do Rio Preto, Brazil.

Srilakshmi Rajagopal (S)

Department of Medical Genetics, Tamil Nadu Dr M.G.R. Medical University, Chennai, India.

Sheela Nampoothiri (S)

Department of Pediatric Genetics, Amrita Institute of Medical Sciences & Research Centre, Cochin, India.

Belinda Campos-Xavier (B)

Division of Genetic Medicine, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Carole Chiesa (C)

Division of Genetic Medicine, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Florence Niel-Bütschi (F)

Division of Genetic Medicine, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Lars Wittler (L)

Department of Developmental Genetics, Max Planck Institute for Molecular Genetics, Berlin, Germany.

Bernd Timmermann (B)

Sequencing Core Facility, Max Planck Institute for Molecular Genetics, Berlin, Germany.

Malte Spielmann (M)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.
Institute for Medical and Human Genetics, Charité-Universitätsmedizin Berlin, Berlin, Germany.
Institut für Humangenetik Lübeck, Universität zu Lübeck, Lübeck, Germany.

Michael I Robson (MI)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.

Alessa Ringel (A)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.

Verena Heinrich (V)

Department of Computational Molecular Biology, Max Planck Institute for Molecular Genetics, Berlin, Germany.

Giulia Cova (G)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.
Institute for Medical and Human Genetics, Charité-Universitätsmedizin Berlin, Berlin, Germany.

Guillaume Andrey (G)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.
Department of Genetic Medicine and Development and iGE3, Faculty of Medicine, University of Geneva, Geneva, Switzerland.

Cesar A Prada-Medina (CA)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany.

Rosanna Pescini-Gobert (R)

Medical Genetics Unit, Department of Computational Biology, University of Lausanne, Lausanne, Switzerland.

Sheila Unger (S)

Division of Genetic Medicine, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Luisa Bonafé (L)

Division of Genetic Medicine, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Phillip Grote (P)

Institute of Cardiovascular Regeneration, Center for Molecular Medicine, Goethe University, Frankfurt am Main, Germany.

Carlo Rivolta (C)

Medical Genetics Unit, Department of Computational Biology, University of Lausanne, Lausanne, Switzerland.
Institute of Molecular and Clinical Ophthalmology Basel (IOB), Basel, Switzerland.
Department of Ophthalmology, University of Basel, Basel, Switzerland.
Department of Genetics and Genome Biology, University of Leicester, Leicester, UK.

Stefan Mundlos (S)

RG Development & Disease, Max Planck Institute for Molecular Genetics, Berlin, Germany. mundlos@molgen.mpg.de.
Institute for Medical and Human Genetics, Charité-Universitätsmedizin Berlin, Berlin, Germany. mundlos@molgen.mpg.de.
Berlin-Brandenburg Center for Regenerative Therapies, Charité-Universitätsmedizin Berlin, Berlin, Germany. mundlos@molgen.mpg.de.

Andrea Superti-Furga (A)

Division of Genetic Medicine, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH