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1. Integrated multi-omics analysis of zinc-finger proteins uncovers roles in RNA regulation

Author

Gosztyla, Maya L., Zhan, Lijun, Olson, Sara, Wei, Xintao, Naritomi, Jack, Nguyen, Grady, Street, Lena, Goda, Grant A., Cavazos, Francisco F., Schmok, Jonathan C., Jain, Manya, Uddin Syed, Easin, Kwon, Eunjeong, Jin, Wenhao, Kofman, Eric, Tankka, Alexandra T., Li, Allison, Gonzalez, Valerie, Lécuyer, Eric, Dominguez, Daniel, Jovanovic, Marko, Graveley, Brenton R., and Yeo, Gene W.

Published
2024
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2. Author Correction: Expanded encyclopaedias of DNA elements in the human and mouse genomes

Author

Moore, Jill E, Purcaro, Michael J, Pratt, Henry E, Epstein, Charles B, Shoresh, Noam, Adrian, Jessika, Kawli, Trupti, Davis, Carrie A, Dobin, Alexander, Kaul, Rajinder, Halow, Jessica, Van Nostrand, Eric L, Freese, Peter, Gorkin, David U, Shen, Yin, He, Yupeng, Mackiewicz, Mark, Pauli-Behn, Florencia, Williams, Brian A, Mortazavi, Ali, Keller, Cheryl A, Zhang, Xiao-Ou, Elhajjajy, Shaimae I, Huey, Jack, Dickel, Diane E, Snetkova, Valentina, Wei, Xintao, Wang, Xiaofeng, Rivera-Mulia, Juan Carlos, Rozowsky, Joel, Zhang, Jing, Chhetri, Surya B, Zhang, Jialing, Victorsen, Alec, White, Kevin P, Visel, Axel, Yeo, Gene W, Burge, Christopher B, Lécuyer, Eric, Gilbert, David M, Dekker, Job, Rinn, John, Mendenhall, Eric M, Ecker, Joseph R, Kellis, Manolis, Klein, Robert J, Noble, William S, Kundaje, Anshul, Guigó, Roderic, Farnham, Peggy J, Cherry, J Michael, Myers, Richard M, Ren, Bing, Graveley, Brenton R, Gerstein, Mark B, Pennacchio, Len A, Snyder, Michael P, Bernstein, Bradley E, Wold, Barbara, Hardison, Ross C, Gingeras, Thomas R, Stamatoyannopoulos, John A, and Weng, Zhiping

Subjects
ENCODE Project Consortium, General Science & Technology
Abstract

In the version of this article initially published, two members of the ENCODE Project Consortium were missing from the author list. Rizi Ai (Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, CA, USA) and Shantao Li (Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT, USA) are now included in the author list. These errors have been corrected in the online version of the article.

Published
2022

4. Persistent mRNA localization defects and cell death in ALS neurons caused by transient cellular stress

Author

Markmiller, Sebastian, Sathe, Shashank, Server, Kari L, Nguyen, Thai B, Fulzele, Amit, Cody, Neal, Javaherian, Ashkan, Broski, Sara, Finkbeiner, Steven, Bennett, Eric J, Lécuyer, Eric, and Yeo, Gene W

Subjects
Biochemistry and Cell Biology, Biological Sciences, ALS, Stem Cell Research - Induced Pluripotent Stem Cell - Human, Genetics, Stem Cell Research, Rare Diseases, Neurodegenerative, Brain Disorders, Neurosciences, Stem Cell Research - Induced Pluripotent Stem Cell, 2.1 Biological and endogenous factors, Neurological, Amyotrophic Lateral Sclerosis, Cell Death, Cytoplasmic Granules, Cytoplasmic Ribonucleoprotein Granules, DNA-Binding Proteins, Humans, Motor Neurons, Mutation, RNA, Messenger, RNA-Binding Proteins, RNA localization, TDP-43, amyotrophic lateral sclerosis, cellular stress response, hnRNPA2B1, motor neurons, neurodegeneration, nucleocytoplasmic transport, protein aggregation, stress granules, RNA Localization, Neurodegeneration, HNRNPA2B1, Medical Physiology, Biological sciences
Abstract

Persistent cytoplasmic aggregates containing RNA binding proteins (RBPs) are central to the pathogenesis of late-onset neurodegenerative disorders such as amyotrophic lateral sclerosis (ALS). These aggregates share components, molecular mechanisms, and cellular protein quality control pathways with stress-induced RNA granules (SGs). Here, we assess the impact of stress on the global mRNA localization landscape of human pluripotent stem cell-derived motor neurons (PSC-MNs) using subcellular fractionation with RNA sequencing and proteomics. Transient stress disrupts subcellular RNA and protein distributions, alters the RNA binding profile of SG- and ALS-relevant RBPs and recapitulates disease-associated molecular changes such as aberrant splicing of STMN2. Although neurotypical PSC-MNs re-establish a normal subcellular localization landscape upon recovery from stress, cells harboring ALS-linked mutations are intransigent and display a delayed-onset increase in neuronal cell death. Our results highlight subcellular molecular distributions as predictive features and underscore the utility of cellular stress as a paradigm to study ALS-relevant mechanisms.

Published
2021

5. A large-scale binding and functional map of human RNA-binding proteins

Author

Van Nostrand, Eric L, Freese, Peter, Pratt, Gabriel A, Wang, Xiaofeng, Wei, Xintao, Xiao, Rui, Blue, Steven M, Chen, Jia-Yu, Cody, Neal AL, Dominguez, Daniel, Olson, Sara, Sundararaman, Balaji, Zhan, Lijun, Bazile, Cassandra, Bouvrette, Louis Philip Benoit, Bergalet, Julie, Duff, Michael O, Garcia, Keri E, Gelboin-Burkhart, Chelsea, Hochman, Myles, Lambert, Nicole J, Li, Hairi, McGurk, Michael P, Nguyen, Thai B, Palden, Tsultrim, Rabano, Ines, Sathe, Shashank, Stanton, Rebecca, Su, Amanda, Wang, Ruth, Yee, Brian A, Zhou, Bing, Louie, Ashley L, Aigner, Stefan, Fu, Xiang-Dong, Lécuyer, Eric, Burge, Christopher B, Graveley, Brenton R, and Yeo, Gene W

Subjects
Biological Sciences, Bioinformatics and Computational Biology, Genetics, Vaccine Related, Immunization, Vaccine Related (AIDS), Prevention, Human Genome, Underpinning research, 1.1 Normal biological development and functioning, Generic health relevance, Alternative Splicing, Base Sequence, Binding Sites, Cell Line, Chromatin, Databases, Genetic, Female, Gene Knockdown Techniques, Humans, Intracellular Space, Male, Protein Binding, RNA, Messenger, RNA-Binding Proteins, Substrate Specificity, Transcriptome, General Science & Technology
Abstract

Many proteins regulate the expression of genes by binding to specific regions encoded in the genome1. Here we introduce a new data set of RNA elements in the human genome that are recognized by RNA-binding proteins (RBPs), generated as part of the Encyclopedia of DNA Elements (ENCODE) project phase III. This class of regulatory elements functions only when transcribed into RNA, as they serve as the binding sites for RBPs that control post-transcriptional processes such as splicing, cleavage and polyadenylation, and the editing, localization, stability and translation of mRNAs. We describe the mapping and characterization of RNA elements recognized by a large collection of human RBPs in K562 and HepG2 cells. Integrative analyses using five assays identify RBP binding sites on RNA and chromatin in vivo, the in vitro binding preferences of RBPs, the function of RBP binding sites and the subcellular localization of RBPs, producing 1,223 replicated data sets for 356 RBPs. We describe the spectrum of RBP binding throughout the transcriptome and the connections between these interactions and various aspects of RNA biology, including RNA stability, splicing regulation and RNA localization. These data expand the catalogue of functional elements encoded in the human genome by the addition of a large set of elements that function at the RNA level by interacting with RBPs.

Published
2020

6. Expanded encyclopaedias of DNA elements in the human and mouse genomes

Author

Moore, Jill E, Purcaro, Michael J, Pratt, Henry E, Epstein, Charles B, Shoresh, Noam, Adrian, Jessika, Kawli, Trupti, Davis, Carrie A, Dobin, Alexander, Kaul, Rajinder, Halow, Jessica, Van Nostrand, Eric L, Freese, Peter, Gorkin, David U, Shen, Yin, He, Yupeng, Mackiewicz, Mark, Pauli-Behn, Florencia, Williams, Brian A, Mortazavi, Ali, Keller, Cheryl A, Zhang, Xiao-Ou, Elhajjajy, Shaimae I, Huey, Jack, Dickel, Diane E, Snetkova, Valentina, Wei, Xintao, Wang, Xiaofeng, Rivera-Mulia, Juan Carlos, Rozowsky, Joel, Zhang, Jing, Chhetri, Surya B, Zhang, Jialing, Victorsen, Alec, White, Kevin P, Visel, Axel, Yeo, Gene W, Burge, Christopher B, Lécuyer, Eric, Gilbert, David M, Dekker, Job, Rinn, John, Mendenhall, Eric M, Ecker, Joseph R, Kellis, Manolis, Klein, Robert J, Noble, William S, Kundaje, Anshul, Guigó, Roderic, Farnham, Peggy J, Cherry, J Michael, Myers, Richard M, Ren, Bing, Graveley, Brenton R, Gerstein, Mark B, Pennacchio, Len A, Snyder, Michael P, Bernstein, Bradley E, Wold, Barbara, Hardison, Ross C, Gingeras, Thomas R, Stamatoyannopoulos, John A, and Weng, Zhiping

Subjects
Biological Sciences, Bioinformatics and Computational Biology, Genetics, Human Genome, 1.1 Normal biological development and functioning, Animals, Chromatin, DNA, DNA Footprinting, DNA Methylation, DNA Replication Timing, Databases, Genetic, Deoxyribonuclease I, Genome, Genome, Human, Genomics, Histones, Humans, Mice, Mice, Transgenic, Molecular Sequence Annotation, RNA-Binding Proteins, Registries, Regulatory Sequences, Nucleic Acid, Transcription, Genetic, Transposases, ENCODE Project Consortium, General Science & Technology
Abstract

The human and mouse genomes contain instructions that specify RNAs and proteins and govern the timing, magnitude, and cellular context of their production. To better delineate these elements, phase III of the Encyclopedia of DNA Elements (ENCODE) Project has expanded analysis of the cell and tissue repertoires of RNA transcription, chromatin structure and modification, DNA methylation, chromatin looping, and occupancy by transcription factors and RNA-binding proteins. Here we summarize these efforts, which have produced 5,992 new experimental datasets, including systematic determinations across mouse fetal development. All data are available through the ENCODE data portal (https://www.encodeproject.org), including phase II ENCODE1 and Roadmap Epigenomics2 data. We have developed a registry of 926,535 human and 339,815 mouse candidate cis-regulatory elements, covering 7.9 and 3.4% of their respective genomes, by integrating selected datatypes associated with gene regulation, and constructed a web-based server (SCREEN; http://screen.encodeproject.org) to provide flexible, user-defined access to this resource. Collectively, the ENCODE data and registry provide an expansive resource for the scientific community to build a better understanding of the organization and function of the human and mouse genomes.

Published
2020

7. Expanded encyclopaedias of DNA elements in the human and mouse genomes.

Author

ENCODE Project Consortium, Moore, Jill E, Purcaro, Michael J, Pratt, Henry E, Epstein, Charles B, Shoresh, Noam, Adrian, Jessika, Kawli, Trupti, Davis, Carrie A, Dobin, Alexander, Kaul, Rajinder, Halow, Jessica, Van Nostrand, Eric L, Freese, Peter, Gorkin, David U, Shen, Yin, He, Yupeng, Mackiewicz, Mark, Pauli-Behn, Florencia, Williams, Brian A, Mortazavi, Ali, Keller, Cheryl A, Zhang, Xiao-Ou, Elhajjajy, Shaimae I, Huey, Jack, Dickel, Diane E, Snetkova, Valentina, Wei, Xintao, Wang, Xiaofeng, Rivera-Mulia, Juan Carlos, Rozowsky, Joel, Zhang, Jing, Chhetri, Surya B, Zhang, Jialing, Victorsen, Alec, White, Kevin P, Visel, Axel, Yeo, Gene W, Burge, Christopher B, Lécuyer, Eric, Gilbert, David M, Dekker, Job, Rinn, John, Mendenhall, Eric M, Ecker, Joseph R, Kellis, Manolis, Klein, Robert J, Noble, William S, Kundaje, Anshul, Guigó, Roderic, Farnham, Peggy J, Cherry, J Michael, Myers, Richard M, Ren, Bing, Graveley, Brenton R, Gerstein, Mark B, Pennacchio, Len A, Snyder, Michael P, Bernstein, Bradley E, Wold, Barbara, Hardison, Ross C, Gingeras, Thomas R, Stamatoyannopoulos, John A, and Weng, Zhiping

Subjects
ENCODE Project Consortium, Chromatin, Animals, Mice, Transgenic, Humans, Mice, Deoxyribonuclease I, Transposases, RNA-Binding Proteins, Histones, DNA, Registries, DNA Footprinting, Genomics, DNA Methylation, DNA Replication Timing, Transcription, Genetic, Regulatory Sequences, Nucleic Acid, Genome, Genome, Human, Databases, Genetic, Molecular Sequence Annotation, Human Genome, HIV/AIDS, Vaccine Related, Biotechnology, Genetics, Immunization, Vaccine Related (AIDS), Prevention, 1.1 Normal biological development and functioning, Generic health relevance, General Science & Technology
Abstract

The human and mouse genomes contain instructions that specify RNAs and proteins and govern the timing, magnitude, and cellular context of their production. To better delineate these elements, phase III of the Encyclopedia of DNA Elements (ENCODE) Project has expanded analysis of the cell and tissue repertoires of RNA transcription, chromatin structure and modification, DNA methylation, chromatin looping, and occupancy by transcription factors and RNA-binding proteins. Here we summarize these efforts, which have produced 5,992 new experimental datasets, including systematic determinations across mouse fetal development. All data are available through the ENCODE data portal (https://www.encodeproject.org), including phase II ENCODE1 and Roadmap Epigenomics2 data. We have developed a registry of 926,535 human and 339,815 mouse candidate cis-regulatory elements, covering 7.9 and 3.4% of their respective genomes, by integrating selected datatypes associated with gene regulation, and constructed a web-based server (SCREEN; http://screen.encodeproject.org) to provide flexible, user-defined access to this resource. Collectively, the ENCODE data and registry provide an expansive resource for the scientific community to build a better understanding of the organization and function of the human and mouse genomes.

Published
2020

8. Context-Dependent and Disease-Specific Diversity in Protein Interactions within Stress Granules

Author

Markmiller, Sebastian, Soltanieh, Sahar, Server, Kari L, Mak, Raymond, Jin, Wenhao, Fang, Mark Y, Luo, En-Ching, Krach, Florian, Yang, Dejun, Sen, Anindya, Fulzele, Amit, Wozniak, Jacob M, Gonzalez, David J, Kankel, Mark W, Gao, Fen-Biao, Bennett, Eric J, Lécuyer, Eric, and Yeo, Gene W

Subjects
Biochemistry and Cell Biology, Biological Sciences, Neurosciences, Brain Disorders, Neurodegenerative, ALS, Rare Diseases, Neurological, Amyotrophic Lateral Sclerosis, Animals, Cytoplasmic Granules, Drosophila melanogaster, HEK293 Cells, HeLa Cells, Humans, Neurons, Protein Interaction Maps, Protein Transport, Ribonucleoproteins, Stress, Physiological, Hela Cells, RNA-binding proteins, amyotrophic lateral sclerosis, granules, heat shock, motor neuron disease, neurodegeneration, phase separation, ribonucleoprotein, stress, Medical and Health Sciences, Developmental Biology, Biological sciences, Biomedical and clinical sciences
Abstract

Stress granules (SGs) are transient ribonucleoprotein (RNP) aggregates that form during cellular stress and are increasingly implicated in human neurodegeneration. To study the proteome and compositional diversity of SGs in different cell types and in the context of neurodegeneration-linked mutations, we used ascorbate peroxidase (APEX) proximity labeling, mass spectrometry, and immunofluorescence to identify ∼150 previously unknown human SG components. A highly integrated, pre-existing SG protein interaction network in unstressed cells facilitates rapid coalescence into larger SGs. Approximately 20% of SG diversity is stress or cell-type dependent, with neuronal SGs displaying a particularly complex repertoire of proteins enriched in chaperones and autophagy factors. Strengthening the link between SGs and neurodegeneration, we demonstrate aberrant dynamics, composition, and subcellular distribution of SGs in cells from amyotrophic lateral sclerosis (ALS) patients. Using three Drosophila ALS/FTD models, we identify SG-associated modifiers of neurotoxicity in vivo. Altogether, our results highlight SG proteins as central to understanding and ultimately targeting neurodegeneration.

Published
2018

11. Resources for the Comprehensive Discovery of Functional RNA Elements

Author

Sundararaman, Balaji, Zhan, Lijun, Blue, Steven M, Stanton, Rebecca, Elkins, Keri, Olson, Sara, Wei, Xintao, Van Nostrand, Eric L, Pratt, Gabriel A, Huelga, Stephanie C, Smalec, Brendan M, Wang, Xiaofeng, Hong, Eurie L, Davidson, Jean M, Lécuyer, Eric, Graveley, Brenton R, and Yeo, Gene W

Subjects
Biological Sciences, Bioinformatics and Computational Biology, Cancer, Biotechnology, Genetics, Binding Sites, Databases, Genetic, Humans, Protein Binding, RNA, RNA, Small Interfering, RNA-Binding Proteins, Transcriptome, Medical and Health Sciences, Developmental Biology, Biological sciences, Biomedical and clinical sciences, Health sciences
Abstract

Transcriptome-wide maps of RNA binding protein (RBP)-RNA interactions by immunoprecipitation (IP)-based methods such as RNA IP (RIP) and crosslinking and IP (CLIP) are key starting points for evaluating the molecular roles of the thousands of human RBPs. A significant bottleneck to the application of these methods in diverse cell lines, tissues, and developmental stages is the availability of validated IP-quality antibodies. Using IP followed by immunoblot assays, we have developed a validated repository of 438 commercially available antibodies that interrogate 365 unique RBPs. In parallel, 362 short-hairpin RNA (shRNA) constructs against 276 unique RBPs were also used to confirm specificity of these antibodies. These antibodies can characterize subcellular RBP localization. With the burgeoning interest in the roles of RBPs in cancer, neurobiology, and development, these resources are invaluable to the broad scientific community. Detailed information about these resources is publicly available at the ENCODE portal (https://www.encodeproject.org/).

Published
2016

14. Dynamics of particulate organic matter composition in coastal systems: Forcing of spatio-temporal variability at multi-systems scale

Author

Liénart, Camilla, Savoye, Nicolas, David, Valérie, Ramond, Pierre, Rodriguez Tress, Paco, Hanquiez, Vincent, Marieu, Vincent, Aubert, Fabien, Aubin, Sébastien, Bichon, Sabrina, Boinet, Christophe, Bourasseau, Line, Bozec, Yann, Bréret, Martine, Breton, Elsa, Caparros, Jocelyne, Cariou, Thierry, Claquin, Pascal, Conan, Pascal, Corre, Anne-Marie, Costes, Laurence, Crouvoisier, Muriel, Del Amo, Yolanda, Derriennic, Hervé, Dindinaud, François, Duran, Robert, Durozier, Maïa, Devesa, Jérémy, Ferreira, Sophie, Feunteun, Eric, Garcia, Nicole, Geslin, Sandrine, Grossteffan, Emilie, Gueux, Aurore, Guillaudeau, Julien, Guillou, Gaël, Jolly, Orianne, Lachaussée, Nicolas, Lafont, Michel, Lagadec, Véronique, Lamoureux, Jézabel, Lauga, Béatrice, Lebreton, Benoît, Lecuyer, Eric, Lehodey, Jean-Paul, Leroux, Cédric, L'Helguen, Stéphane, Macé, Eric, Maria, Eric, Mousseau, Laure, Nowaczyk, Antoine, Pineau, Philippe, Petit, Franck, Pujo-Pay, Mireille, Raimbault, Patrick, Rimmelin-Maury, Peggy, Rouaud, Vanessa, Sauriau, Pierre-Guy, Sultan, Emmanuelle, and Susperregui, Nicolas

Published
2018
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15. Dynamics of particulate organic matter composition in coastal systems: A spatio-temporal study at multi-systems scale

Author

Liénart, Camilla, Savoye, Nicolas, Bozec, Yann, Breton, Elsa, Conan, Pascal, David, Valérie, Feunteun, Eric, Grangeré, Karine, Kerhervé, Philippe, Lebreton, Benoît, Lefebvre, Sébastien, L'Helguen, Stéphane, Mousseau, Laure, Raimbault, Patrick, Richard, Pierre, Riera, Pascal, Sauriau, Pierre-Guy, Schaal, Gauthier, Aubert, Fabien, Aubin, Sébastien, Bichon, Sabrina, Boinet, Christophe, Bourasseau, Line, Bréret, Martine, Caparros, Jocelyne, Cariou, Thierry, Charlier, Karine, Claquin, Pascal, Cornille, Vincent, Corre, Anne-Marie, Costes, Laurence, Crispi, Olivier, Crouvoisier, Muriel, Czamanski, Marie, Del Amo, Yolanda, Derriennic, Hervé, Dindinaud, François, Durozier, Maïa, Hanquiez, Vincent, Nowaczyk, Antoine, Devesa, Jérémy, Ferreira, Sophie, Fornier, Michel, Garcia, Fabrice, Garcia, Nicole, Geslin, Sandrine, Grossteffan, Emilie, Gueux, Aurore, Guillaudeau, Julien, Guillou, Gaël, Joly, Orianne, Lachaussée, Nicolas, Lafont, Michel, Lamoureux, Jézabel, Lecuyer, Eric, Lehodey, Jean-Paul, Lemeille, David, Leroux, Cédric, Macé, Eric, Maria, Eric, Pineau, Philippe, Petit, Franck, Pujo-Pay, Mireille, Rimelin-Maury, Peggy, and Sultan, Emmanuelle

Published
2017
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18. Author Correction: A large-scale binding and functional map of human RNA-binding proteins

Author

Van Nostrand, Eric L., Freese, Peter, Pratt, Gabriel A., Wang, Xiaofeng, Wei, Xintao, Xiao, Rui, Blue, Steven M., Chen, Jia-Yu, Cody, Neal A. L., Dominguez, Daniel, Olson, Sara, Sundararaman, Balaji, Zhan, Lijun, Bazile, Cassandra, Bouvrette, Louis Philip Benoit, Bergalet, Julie, Duff, Michael O., Garcia, Keri E., Gelboin-Burkhart, Chelsea, Hochman, Myles, Lambert, Nicole J., Li, Hairi, McGurk, Michael P., Nguyen, Thai B., Palden, Tsultrim, Rabano, Ines, Sathe, Shashank, Stanton, Rebecca, Su, Amanda, Wang, Ruth, Yee, Brian A., Zhou, Bing, Louie, Ashley L., Aigner, Stefan, Fu, Xiang-Dong, Lécuyer, Eric, Burge, Christopher B., Graveley, Brenton R., and Yeo, Gene W.

Published
2021
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19. RBP Image Database: A resource for the systematic characterization of the subcellular distribution properties of human RNA binding proteins

Author

Benoit Bouvrette, Louis Philip, primary, Wang, Xiaofeng, additional, Boulais, Jonathan, additional, Kong, Jian, additional, Syed, Easin Uddin, additional, Blue, Steven M, additional, Zhan, Lijun, additional, Olson, Sara, additional, Stanton, Rebecca, additional, Wei, Xintao, additional, Yee, Brian, additional, Van Nostrand, Eric L, additional, Fu, Xiang-Dong, additional, Burge, Christopher B, additional, Graveley, Brenton R, additional, Yeo, Gene W, additional, and Lécuyer, Eric, additional

Published
2022
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20. Author Correction: Expanded encyclopaedias of DNA elements in the human and mouse genomes

Author

ENCODE Project Consortium, Moore, Jill E, Purcaro, Michael J, Pratt, Henry E, Epstein, Charles B, Shoresh, Noam, Adrian, Jessika, Kawli, Trupti, Davis, Carrie A, Dobin, Alexander, Kaul, Rajinder, Halow, Jessica, Van Nostrand, Eric L, Freese, Peter, Gorkin, David U, Shen, Yin, He, Yupeng, Mackiewicz, Mark, Pauli-Behn, Florencia, Williams, Brian A, Mortazavi, Ali, Keller, Cheryl A, Zhang, Xiao-Ou, Elhajjajy, Shaimae I, Huey, Jack, Dickel, Diane E, Snetkova, Valentina, Wei, Xintao, Wang, Xiaofeng, Rivera-Mulia, Juan Carlos, Rozowsky, Joel, Zhang, Jing, Chhetri, Surya B, Zhang, Jialing, Victorsen, Alec, White, Kevin P, Visel, Axel, Yeo, Gene W, Burge, Christopher B, Lécuyer, Eric, Gilbert, David M, Dekker, Job, Rinn, John, Mendenhall, Eric M, Ecker, Joseph R, Kellis, Manolis, Klein, Robert J, Noble, William S, Kundaje, Anshul, Guigó, Roderic, Farnham, Peggy J, Cherry, J Michael, Myers, Richard M, Ren, Bing, Graveley, Brenton R, Gerstein, Mark B, Pennacchio, Len A, Snyder, Michael P, Bernstein, Bradley E, Wold, Barbara, Hardison, Ross C, Gingeras, Thomas R, Stamatoyannopoulos, John A, and Weng, Zhiping

Subjects
ENCODE Project Consortium, General Science & Technology
Abstract

In the version of this article initially published, two members of the ENCODE Project Consortium were missing from the author list. Rizi Ai (Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, CA, USA) and Shantao Li (Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT, USA) are now included in the author list. These errors have been corrected in the online version of the article.

Published
2022

21. RBP Image Database: A resource for the systematic characterization of the subcellular distribution properties of human RNA binding proteins

Author

Massachusetts Institute of Technology. Department of Biology, Benoit Bouvrette, Louis Philip, Wang, Xiaofeng, Boulais, Jonathan, Kong, Jian, Syed, Easin Uddin, Blue, Steven M, Zhan, Lijun, Olson, Sara, Stanton, Rebecca, Wei, Xintao, Yee, Brian, Van Nostrand, Eric L, Fu, Xiang-Dong, Burge, Christopher B, Graveley, Brenton R, Yeo, Gene W, Lécuyer, Eric, Massachusetts Institute of Technology. Department of Biology, Benoit Bouvrette, Louis Philip, Wang, Xiaofeng, Boulais, Jonathan, Kong, Jian, Syed, Easin Uddin, Blue, Steven M, Zhan, Lijun, Olson, Sara, Stanton, Rebecca, Wei, Xintao, Yee, Brian, Van Nostrand, Eric L, Fu, Xiang-Dong, Burge, Christopher B, Graveley, Brenton R, Yeo, Gene W, and Lécuyer, Eric

Abstract

Abstract RNA binding proteins (RBPs) are central regulators of gene expression implicated in all facets of RNA metabolism. As such, they play key roles in cellular physiology and disease etiology. Since different steps of post-transcriptional gene expression tend to occur in specific regions of the cell, including nuclear or cytoplasmic locations, defining the subcellular distribution properties of RBPs is an important step in assessing their potential functions. Here, we present the RBP Image Database, a resource that details the subcellular localization features of 301 RBPs in the human HepG2 and HeLa cell lines, based on the results of systematic immuno-fluorescence studies conducted using a highly validated collection of RBP antibodies and a panel of 12 markers for specific organelles and subcellular structures. The unique features of the RBP Image Database include: (i) hosting of comprehensive representative images for each RBP-marker pair, with ∼250,000 microscopy images; (ii) a manually curated controlled vocabulary of annotation terms detailing the localization features of each factor; and (iii) a user-friendly interface allowing the rapid querying of the data by target or annotation. The RBP Image Database is freely available at https://rnabiology.ircm.qc.ca/RBPImage/.

Published
2022

25. Expanded encyclopaedias of DNA elements in the human and mouse genomes

Author

Moore, Jill E., Purcaro, Michael J., Pratt, Henry E., Epstein, Charles B., Shoresh, Noam, Adrian, Jessika, Kawli, Trupti, Davis, Carrie A., Dobin, Alexander, Kaul, Rajinder, Halow, Jessica, Van Nostrand, Eric L., Freese, Peter Dale, Gorkin, David U., Shen, Yin, He, Yupeng, Mackiewicz, Mark, Pauli-Behn, Florencia, Williams, Brian A., Mortazavi, Ali, Keller, Cheryl A., Zhang, Xiao-Ou, Elhajjajy, Shaimae I., Huey, Jack, Dickel, Diane E., Snetkova, Valentina, Wei, Xintao, Wang, Xiaofeng, Rivera-Mulia, Juan Carlos, Rozowsky, Joel, Zhang, Jing, Chhetri, Surya B., Zhang, Jialing, Victorsen, Alec, White, Kevin P., Visel, Axel, Yeo, Gene W., Burge, Christopher B, Lécuyer, Eric, Gilbert, David M., Dekker, Job, Rinn, John, Mendenhall, Eric M., Ecker, Joseph R., Kellis, Manolis, Klein, Robert J., Noble, William S., Kundaje, Anshul, Guigó, Roderic, Farnham, Peggy J., Cherry, J. Michael, Myers, Richard M., Ren, Bing, Graveley, Brenton R., Gerstein, Mark B., Pennacchio, Len A., Snyder, Michael P., Bernstein, Bradley E., Wold, Barbara, Hardison, Ross C., Gingeras, Thomas R., Stamatoyannopoulos, John A., Weng, Zhiping, Moore, Jill E., Purcaro, Michael J., Pratt, Henry E., Epstein, Charles B., Shoresh, Noam, Adrian, Jessika, Kawli, Trupti, Davis, Carrie A., Dobin, Alexander, Kaul, Rajinder, Halow, Jessica, Van Nostrand, Eric L., Freese, Peter Dale, Gorkin, David U., Shen, Yin, He, Yupeng, Mackiewicz, Mark, Pauli-Behn, Florencia, Williams, Brian A., Mortazavi, Ali, Keller, Cheryl A., Zhang, Xiao-Ou, Elhajjajy, Shaimae I., Huey, Jack, Dickel, Diane E., Snetkova, Valentina, Wei, Xintao, Wang, Xiaofeng, Rivera-Mulia, Juan Carlos, Rozowsky, Joel, Zhang, Jing, Chhetri, Surya B., Zhang, Jialing, Victorsen, Alec, White, Kevin P., Visel, Axel, Yeo, Gene W., Burge, Christopher B, Lécuyer, Eric, Gilbert, David M., Dekker, Job, Rinn, John, Mendenhall, Eric M., Ecker, Joseph R., Kellis, Manolis, Klein, Robert J., Noble, William S., Kundaje, Anshul, Guigó, Roderic, Farnham, Peggy J., Cherry, J. Michael, Myers, Richard M., Ren, Bing, Graveley, Brenton R., Gerstein, Mark B., Pennacchio, Len A., Snyder, Michael P., Bernstein, Bradley E., Wold, Barbara, Hardison, Ross C., Gingeras, Thomas R., Stamatoyannopoulos, John A., and Weng, Zhiping

Abstract

The human and mouse genomes contain instructions that specify RNAs and proteins and govern the timing, magnitude, and cellular context of their production. To better delineate these elements, phase III of the Encyclopedia of DNA Elements (ENCODE) Project has expanded analysis of the cell and tissue repertoires of RNA transcription, chromatin structure and modification, DNA methylation, chromatin looping, and occupancy by transcription factors and RNA-binding proteins. Here we summarize these efforts, which have produced 5,992 new experimental datasets, including systematic determinations across mouse fetal development. All data are available through the ENCODE data portal (https://www.encodeproject.org), including phase II ENCODE1 and Roadmap Epigenomics2 data. We have developed a registry of 926,535 human and 339,815 mouse candidate cis-regulatory elements, covering 7.9 and 3.4% of their respective genomes, by integrating selected datatypes associated with gene regulation, and constructed a web-based server (SCREEN; http://screen.encodeproject.org) to provide flexible, user-defined access to this resource. Collectively, the ENCODE data and registry provide an expansive resource for the scientific community to build a better understanding of the organization and function of the human and mouse genomes., NIH (Grants U01HG007019, U01HG007033, U01HG007036, U01HG007037, U41HG006992, U41HG006993, U41HG006994, U41HG006995, U41HG006996, U41HG006997, U41HG006998, U41HG006999, U41HG007000, U41HG007001, U41HG007002, U41HG007003, U54HG006991, U54HG006997, U54HG006998, U54HG007004, U54HG007005, U54HG007010 and UM1HG009442)

Published
2021

26. WEB SITE WISDOM

Author

Sanford, Jeff, Joyce, Jim, Lecuyer, Eric R., Tarker, Ray, Engel, Peter, Matheson, Ron, Drohobyczer, Alex, Sullivan, Tim, and Sharp, Steven D.

Published
1997

27. Pervasive Chromatin-RNA Binding Protein Interactions Enable RNA-Based Regulation of Transcription

Author

Massachusetts Institute of Technology. Computational and Systems Biology Program, Xiao, Rui, Chen, Jia-Yu, Liang, Zhengyu, Luo, Daji, Chen, Geng, Lu, Zhi John, Chen, Yang, Zhou, Bing, Li, Hairi, Du, Xian, Yang, Yang, San, Mingkui, Wei, Xintao, Liu, Wen, Lécuyer, Eric, Graveley, Brenton R., Yeo, Gene W., Burge, Christopher B, Zhang, Michael Q., Zhou, Yu, Fu, Xiang-Dong, Massachusetts Institute of Technology. Computational and Systems Biology Program, Xiao, Rui, Chen, Jia-Yu, Liang, Zhengyu, Luo, Daji, Chen, Geng, Lu, Zhi John, Chen, Yang, Zhou, Bing, Li, Hairi, Du, Xian, Yang, Yang, San, Mingkui, Wei, Xintao, Liu, Wen, Lécuyer, Eric, Graveley, Brenton R., Yeo, Gene W., Burge, Christopher B, Zhang, Michael Q., Zhou, Yu, and Fu, Xiang-Dong

Abstract

Increasing evidence suggests that transcriptional control and chromatin activities at large involve regulatory RNAs, which likely enlist specific RNA-binding proteins (RBPs). Although multiple RBPs have been implicated in transcription control, it has remained unclear how extensively RBPs directly act on chromatin. We embarked on a large-scale RBP ChIP-seq analysis, revealing widespread RBP presence in active chromatin regions in the human genome. Like transcription factors (TFs), RBPs also show strong preference for hotspots in the genome, particularly gene promoters, where their association is frequently linked to transcriptional output. Unsupervised clustering reveals extensive co-association between TFs and RBPs, as exemplified by YY1, a known RNA-dependent TF, and RBM25, an RBP involved in splicing regulation. Remarkably, RBM25 depletion attenuates all YY1-dependent activities, including chromatin binding, DNA looping, and transcription. We propose that various RBPs may enhance network interaction through harnessing regulatory RNAs to control transcription. Nuclear RNA-binding proteins are pervasive at gene promoters, with many directly participating in transcription through functional interaction with specific transcription factors.

Published
2020

33. Persistent mRNA Localization Defects and Cell Death in ALS Neurons Caused by Transient Cellular Stress

Author

Markmiller, Sebastian, primary, Sathe, Shashank, additional, Server, Kari L., additional, Nguyen, Thai B., additional, Fulzele, Amit, additional, Cody, Neal, additional, Javaherian, Ashkan, additional, Broski, Sara, additional, Finkbeiner, Steven, additional, Bennett, Eric, additional, Lécuyer, Eric, additional, and Yeo, Gene W., additional

Published
2020
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36. Pervasive Chromatin-RNA Binding Protein Interactions Enable RNA-Based Regulation of Transcription

Author

Xiao, Rui, primary, Chen, Jia-Yu, additional, Liang, Zhengyu, additional, Luo, Daji, additional, Chen, Geng, additional, Lu, Zhi John, additional, Chen, Yang, additional, Zhou, Bing, additional, Li, Hairi, additional, Du, Xian, additional, Yang, Yang, additional, San, Mingkui, additional, Wei, Xintao, additional, Liu, Wen, additional, Lécuyer, Eric, additional, Graveley, Brenton R., additional, Yeo, Gene W., additional, Burge, Christopher B., additional, Zhang, Michael Q., additional, Zhou, Yu, additional, and Fu, Xiang-Dong, additional

Published
2019
Full Text
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40. Context‐dependent and Disease‐specific Diversity in Stress Granules Formed from Pre‐existing Protein Interactions

Author

Markmiller, Sebastian, primary, Soltanieh, Sahar, additional, Server, Kari L., additional, Mak, Raymond, additional, Jin, Wenhao, additional, Fang, Mark Y., additional, Luo, En‐Ching, additional, Yeo, Gene W., additional, Krach, Florian, additional, Yang, Dejun, additional, Sen, Anindya, additional, Fulzele, Amit, additional, Wozniak, Jacob M., additional, Gonzalez, David J., additional, Kankel, Mark W., additional, Gao, Fen‐Biao, additional, Bennett, Eric J., additional, and Lécuyer, Eric, additional

Published
2018
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48. Resources for the Comprehensive Discovery of Functional RNA Elements.

Author

Zhan, Lijun, Zhan, Lijun, Blue, Steven, Stanton, Rebecca, Elkins, Keri, Olson, Sara, Wei, Xintao, Van Nostrand, Eric, Pratt, Gabriel, Huelga, Stephanie, Smalec, Brendan, Wang, Xiaofeng, Hong, Eurie, Davidson, Jean, Lécuyer, Eric, Graveley, Brenton, Yeo, Gene, Sundararaman, Balaji, Zhan, Lijun, Zhan, Lijun, Blue, Steven, Stanton, Rebecca, Elkins, Keri, Olson, Sara, Wei, Xintao, Van Nostrand, Eric, Pratt, Gabriel, Huelga, Stephanie, Smalec, Brendan, Wang, Xiaofeng, Hong, Eurie, Davidson, Jean, Lécuyer, Eric, Graveley, Brenton, Yeo, Gene, and Sundararaman, Balaji

Abstract

Transcriptome-wide maps of RNA binding protein (RBP)-RNA interactions by immunoprecipitation (IP)-based methods such as RNA IP (RIP) and crosslinking and IP (CLIP) are key starting points for evaluating the molecular roles of the thousands of human RBPs. A significant bottleneck to the application of these methods in diverse cell lines, tissues, and developmental stages is the availability of validated IP-quality antibodies. Using IP followed by immunoblot assays, we have developed a validated repository of 438 commercially available antibodies that interrogate 365 unique RBPs. In parallel, 362 short-hairpin RNA (shRNA) constructs against 276 unique RBPs were also used to confirm specificity of these antibodies. These antibodies can characterize subcellular RBP localization. With the burgeoning interest in the roles of RBPs in cancer, neurobiology, and development, these resources are invaluable to the broad scientific community. Detailed information about these resources is publicly available at the ENCODE portal (https://www.encodeproject.org/).

Published
2016

50. Transcriptome-wide Regulation of Pre-mRNA Splicing and mRNA Localization by Muscleblind Proteins

Author

Harvard University--MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology. Department of Biological Engineering, Massachusetts Institute of Technology. Department of Biology, Koch Institute for Integrative Cancer Research at MIT, Wang, Eric Tzy-shi, Wang, Thomas, Treacy, Daniel J., Housman, David E., Burge, Christopher B., Cody, Neal A. L., Jog, Sonali, Biancolella, Michela, Wang, Thomas T., Luo, Shujun, Schroth, Gary P., Reddy, Sita, Lécuyer, Eric, Housman, David E, Burge, Christopher B, Wang, Eric T, Harvard University--MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology. Department of Biological Engineering, Massachusetts Institute of Technology. Department of Biology, Koch Institute for Integrative Cancer Research at MIT, Wang, Eric Tzy-shi, Wang, Thomas, Treacy, Daniel J., Housman, David E., Burge, Christopher B., Cody, Neal A. L., Jog, Sonali, Biancolella, Michela, Wang, Thomas T., Luo, Shujun, Schroth, Gary P., Reddy, Sita, Lécuyer, Eric, Housman, David E, Burge, Christopher B, and Wang, Eric T

Abstract

The muscleblind-like (Mbnl) family of RNA-binding proteins plays important roles in muscle and eye development and in myotonic dystrophy (DM), in which expanded CUG or CCUG repeats functionally deplete Mbnl proteins. We identified transcriptome-wide functional and biophysical targets of Mbnl proteins in brain, heart, muscle, and myoblasts by using RNA-seq and CLIP-seq approaches. This analysis identified several hundred splicing events whose regulation depended on Mbnl function in a pattern indicating functional interchangeability between Mbnl1 and Mbnl2. A nucleotide resolution RNA map associated repression or activation of exon splicing with Mbnl binding near either 3′ splice site or near the downstream 5′ splice site, respectively. Transcriptomic analysis of subcellular compartments uncovered a global role for Mbnls in regulating localization of mRNAs in both mouse and Drosophila cells, and Mbnl-dependent translation and protein secretion were observed for a subset of mRNAs with Mbnl-dependent localization. These findings hold several new implications for DM pathogenesis., Massachusetts Institute of Technology (Poitras Fellowship), National Science Foundation (U.S.) (equipment grant no. 082139), National Institutes of Health (U.S.)

Published
2014

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