A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis

Pimentel, Harold; Parra, Marilyn; Gee, Sherry L.; Mohandas, Narla; Pachter, Lior; Conboy, John G.

doi:10.1093/nar/gkv1168

Title: A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis

Journal Article · Tue Nov 03 00:00:00 EST 2015 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkv1168· OSTI ID:1256072

Pimentel, Harold ^[1]; Parra, Marilyn ^[2]; Gee, Sherry L. ^[2]; Mohandas, Narla ^[3]; Pachter, Lior ^[1]; Conboy, John G. ^[2]

Univ. of California, Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
New York Blood Center, New York, NY (United States). Red Cell Physiology Laboratory

Differentiating erythroblasts execute a dynamic alternative splicing program shown here to include extensive and diverse intron retention (IR) events. Cluster analysis revealed hundreds of developmentally-dynamic introns that exhibit increased IR in mature erythroblasts, and are enriched in functions related to RNA processing such as SF3B1 spliceosomal factor. Distinct, developmentally-stable IR clusters are enriched in metal-ion binding functions and include mitoferrin genes SLC25A37 and SLC25A28 that are critical for iron homeostasis. Some IR transcripts are abundant, e.g. comprising ~50% of highly-expressed SLC25A37 and SF3B1 transcripts in late erythroblasts, and thereby limiting functional mRNA levels. IR transcripts tested were predominantly nuclear-localized. Splice site strength correlated with IR among stable but not dynamic intron clusters, indicating distinct regulation of dynamically-increased IR in late erythroblasts. Retained introns were preferentially associated with alternative exons with premature termination codons (PTCs). High IR was observed in disease-causing genes including SF3B1 and the RNA binding protein FUS. Comparative studies demonstrated that the intron retention program in erythroblasts shares features with other tissues but ultimately is unique to erythropoiesis. We conclude that IR is a multi-dimensional set of processes that post-transcriptionally regulate diverse gene groups during normal erythropoiesis, misregulation of which could be responsible for human disease.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH1123; AC02-05CH11231

OSTI ID:: 1256072

Alternate ID(s):: OSTI ID: 1379053

Journal Information:: Nucleic Acids Research, Vol. 44, Issue 2; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 118 works

Citation information provided by
Web of Science

References (48)

Aberrant splicing of U12-type introns is the hallmark of ZRSR2 mutant myelodysplastic syndrome Madan, Vikas; Kanojia, Deepika; Li, Jia Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7042	journal	January 2015
Stress-responsive maturation of Clk1/4 pre-mRNAs promotes phosphorylation of SR splicing factor Ninomiya, Kensuke; Kataoka, Naoyuki; Hagiwara, Masatoshi The Journal of Cell Biology, Vol. 195, Issue 1 https://doi.org/10.1083/jcb.201107093	journal	September 2011
Developmental transcriptome analysis of human erythropoiesis Shi, L.; Lin, Y. -H.; Sierant, M. C. Human Molecular Genetics, Vol. 23, Issue 17 https://doi.org/10.1093/hmg/ddu167	journal	April 2014
Global transcriptome analyses of human and murine terminal erythroid differentiation An, Xiuli; Schulz, Vincent P.; Li, Jie Blood, Vol. 123, Issue 22 https://doi.org/10.1182/blood-2014-01-548305	journal	May 2014
Removal of Retained Introns Regulates Translation in the Rapidly Developing Gametophyte of Marsilea vestita Boothby, Thomas C.; Zipper, Richard S.; van der Weele, Corine M. Developmental Cell, Vol. 24, Issue 5 https://doi.org/10.1016/j.devcel.2013.01.015	journal	March 2013
Maximum Entropy Modeling of Short Sequence Motifs with Applications to RNA Splicing Signals Yeo, Gene; Burge, Christopher B. Journal of Computational Biology, Vol. 11, Issue 2-3 https://doi.org/10.1089/1066527041410418	journal	March 2004
Co-transcriptional splicing of constitutive and alternative exons Pandya-Jones, A.; Black, D. L. RNA, Vol. 15, Issue 10 https://doi.org/10.1261/rna.1714509	journal	August 2009
Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements Lareau, Liana F.; Inada, Maki; Green, Richard E. Nature, Vol. 446, Issue 7138 https://doi.org/10.1038/nature05676	journal	March 2007
Isolation and functional characterization of human erythroblasts at distinct stages: implications for understanding of normal and disordered erythropoiesis in vivo Hu, Jingping; Liu, Jing; Xue, Fumin Blood, Vol. 121, Issue 16 https://doi.org/10.1182/blood-2013-01-476390	journal	April 2013
Orchestrated Intron Retention Regulates Normal Granulocyte Differentiation Wong, Justin J. -L.; Ritchie, William; Ebner, Olivia A. Cell, Vol. 154, Issue 3 https://doi.org/10.1016/j.cell.2013.06.052	journal	August 2013
Erythroid mRNA processing: a “splice of life” Wojchowski, Don M. Blood, Vol. 124, Issue 4 https://doi.org/10.1182/blood-2014-06-579649	journal	July 2014
Streaming fragment assignment for real-time analysis of sequencing experiments Roberts, Adam; Pachter, Lior Nature Methods, Vol. 10, Issue 1 https://doi.org/10.1038/nmeth.2251	journal	November 2012
NOVA-dependent regulation of cryptic NMD exons controls synaptic protein levels after seizure Eom, Taesun; Zhang, Chaolin; Wang, Huidong eLife, Vol. 2 https://doi.org/10.7554/elife.00178	journal	January 2013
A dynamic alternative splicing program regulates gene expression during terminal erythropoiesis Pimentel, Harold; Parra, Marilyn; Gee, Sherry Nucleic Acids Research, Vol. 42, Issue 6 https://doi.org/10.1093/nar/gkt1388	journal	January 2014
Widespread intron retention diversifies most cancer transcriptomes Dvinge, Heidi; Bradley, Robert K. Genome Medicine, Vol. 7, Issue 1 https://doi.org/10.1186/s13073-015-0168-9	journal	May 2015
Coordinated regulation of neuronal mRNA steady-state levels through developmentally controlled intron retention Yap, K.; Lim, Z. Q.; Khandelia, P. Genes & Development, Vol. 26, Issue 11 https://doi.org/10.1101/gad.188037.112	journal	June 2012
RNA-Seq gene expression estimation with read mapping uncertainty Li, Bo; Ruotti, Victor; Stewart, Ron M. Bioinformatics, Vol. 26, Issue 4 https://doi.org/10.1093/bioinformatics/btp692	journal	December 2009
Splicing kinetics and transcript release from the chromatin compartment limit the rate of Lipid A-induced gene expression Pandya-Jones, A.; Bhatt, D. M.; Lin, C. -H. RNA, Vol. 19, Issue 6 https://doi.org/10.1261/rna.039081.113	journal	April 2013
Detained introns are a novel, widespread class of post-transcriptionally spliced introns Boutz, Paul L.; Bhutkar, Arjun; Sharp, Phillip A. Genes & Development, Vol. 29, Issue 1 https://doi.org/10.1101/gad.247361.114	journal	January 2015
Regulation of Splicing Factors by Alternative Splicing and NMD Is Conserved between Kingdoms Yet Evolutionarily Flexible Lareau, Liana F.; Brenner, Steven E. Molecular Biology and Evolution, Vol. 32, Issue 4 https://doi.org/10.1093/molbev/msv002	journal	March 2015
U1 snRNA Directly Interacts with Polypyrimidine Tract-Binding Protein during Splicing Repression Sharma, Shalini; Maris, Christophe; Allain, Frédéric H. -T. Molecular Cell, Vol. 41, Issue 5 https://doi.org/10.1016/j.molcel.2011.02.012	journal	March 2011
Adipose-derived mesenchymal stem cells differentiate into heterogeneous cancer-associated fibroblasts in a stroma-rich xenograft model Miyazaki, Yoshihiro; Oda, Tatsuya; Inagaki, Yuki Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-84058-3	journal	February 2021
Lineage and species-specific long noncoding RNAs during erythro-megakaryocytic development Paralkar, Vikram R.; Mishra, Tejaswini; Luan, Jing Blood, Vol. 123, Issue 12 https://doi.org/10.1182/blood-2013-12-544494	journal	March 2014
Cotranscriptional splicing efficiency differs dramatically between Drosophila and mouse Khodor, Y. L.; Menet, J. S.; Tolan, M. RNA, Vol. 18, Issue 12 https://doi.org/10.1261/rna.034090.112	journal	October 2012
The RNA-binding protein hnRNPLL induces a T cell alternative splicing program delineated by differential intron retention in polyadenylated RNA Cho, Vicky; Mei, Yan; Sanny, Arleen Genome Biology, Vol. 15, Issue 1 https://doi.org/10.1186/gb-2014-15-1-r26	journal	January 2014
Caspase-2 pre-mRNA alternative splicing: Identification of an intronic element containing a decoy 3' acceptor site Cote, J.; Dupuis, S.; Jiang, Z. -H. Proceedings of the National Academy of Sciences, Vol. 98, Issue 3 https://doi.org/10.1073/pnas.98.3.938	journal	January 2001
PSD-95 is post-transcriptionally repressed during early neural development by PTBP1 and PTBP2 Zheng, Sika; Gray, Erin E.; Chawla, Geetanjali Nature Neuroscience, Vol. 15, Issue 3 https://doi.org/10.1038/nn.3026	journal	January 2012
HnRNP L and HnRNP A1 Induce Extended U1 snRNA Interactions with an Exon to Repress Spliceosome Assembly Chiou, Ni-Ting; Shankarling, Ganesh; Lynch, Kristen W. Molecular Cell, Vol. 49, Issue 5 https://doi.org/10.1016/j.molcel.2012.12.025	journal	March 2013
Differentiation-associated switches in protein 4.1 expression. Synthesis of multiple structural isoforms during normal human erythropoiesis. Chasis, J. A.; Coulombel, L.; Conboy, J. Journal of Clinical Investigation, Vol. 91, Issue 1 https://doi.org/10.1172/JCI116189	journal	January 1993
Novel Functions for the Endocytic Regulatory Proteins MICAL-L1 and EHD1 in Mitosis Reinecke, James B.; Katafiasz, Dawn; Naslavsky, Naava Traffic, Vol. 16, Issue 1 https://doi.org/10.1111/tra.12234	journal	November 2014
Death by Splicing: Tumor Suppressor RBM5 Freezes Splice-Site Pairing Kotlajich, Matthew V.; Hertel, Klemens J. Molecular Cell, Vol. 32, Issue 2 https://doi.org/10.1016/j.molcel.2008.10.008	journal	October 2008
RBM5/Luca-15/H37 Regulates Fas Alternative Splice Site Pairing after Exon Definition Bonnal, Sophie; Martínez, Concepción; Förch, Patrik Molecular Cell, Vol. 32, Issue 1 https://doi.org/10.1016/j.molcel.2008.08.008	journal	October 2008
Distinct iron architecture in SF3B1-mutant myelodysplastic syndrome patients is linked to an SLC25A37 splice variant with a retained intron Visconte, V.; Avishai, N.; Mahfouz, R. Leukemia, Vol. 29, Issue 1 https://doi.org/10.1038/leu.2014.170	journal	May 2014
Of mice and men… Palis, James Blood, Vol. 123, Issue 22 https://doi.org/10.1182/blood-2014-04-565457	journal	May 2014
Tissue-specific alternative splicing of protein 4.1 inserts an exon necessary for formation of the ternary complex with erythrocyte spectrin and F-actin Horne, Wc; Huang, Sc; Becker, Ps Blood, Vol. 82, Issue 8 https://doi.org/10.1182/blood.v82.8.2558.bloodjournal8282558	journal	October 1993
Widespread intron retention in mammals functionally tunes transcriptomes Braunschweig, Ulrich; Barbosa-Morais, Nuno L.; Pan, Qun Genome Research, Vol. 24, Issue 11 https://doi.org/10.1101/gr.177790.114	journal	September 2014
Widespread Regulation of Translation by Elongation Pausing in Heat Shock Shalgi, Reut; Hurt, Jessica A.; Krykbaeva, Irina Molecular Cell, Vol. 49, Issue 3 https://doi.org/10.1016/j.molcel.2012.11.028	journal	February 2013
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
Separase-dependent cleavage of pericentrin B is necessary and sufficient for centriole disengagement during mitosis Lee, Kwanwoo; Rhee, Kunsoo Cell Cycle, Vol. 11, Issue 13 https://doi.org/10.4161/cc.20878	journal	July 2012
Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nucleic Acids Research, Vol. 37, Issue 1 https://doi.org/10.1093/nar/gkn923	journal	November 2008
RNA sequencing of cancer reveals novel splicing alterations Eswaran, Jeyanthy; Horvath, Anelia; Godbole, Sucheta Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep01689	journal	April 2013
REEP3/4 Ensure Endoplasmic Reticulum Clearance from Metaphase Chromatin and Proper Nuclear Envelope Architecture Schlaitz, Anne-Lore; Thompson, James; Wong, Catherine C. L. Developmental Cell, Vol. 26, Issue 3 https://doi.org/10.1016/j.devcel.2013.06.016	journal	August 2013
Comprehensive splicing functional analysis of DNA variants of the BRCA2 gene by hybrid minigenes Acedo, Alberto; Sanz, David J.; Durán, Mercedes Breast Cancer Research, Vol. 14, Issue 3 https://doi.org/10.1186/bcr3202	journal	May 2012
PREEParing for Mitosis Burke, Brian Developmental Cell, Vol. 26, Issue 3 https://doi.org/10.1016/j.devcel.2013.07.018	journal	August 2013
Tissue-specific alternative splicing of protein 4.1 inserts an exon necessary for formation of the ternary complex with erythrocyte spectrin and F-actin Horne, Wc; Huang, Sc; Becker, Ps Blood, Vol. 82, Issue 8 https://doi.org/10.1182/blood.V82.8.2558.2558	journal	October 1993
Genome-wide mapping of alternative splicing in Arabidopsis thaliana Filichkin, S. A.; Priest, H. D.; Givan, S. A. Genome Research, Vol. 20, Issue 1 https://doi.org/10.1101/gr.093302.109	journal	October 2009
Muscleblind-like 1 (Mbnl1) regulates pre-mRNA alternative splicing during terminal erythropoiesis Cheng, Albert W.; Shi, Jiahai; Wong, Piu Blood, Vol. 124, Issue 4 https://doi.org/10.1182/blood-2013-12-542209	journal	July 2014
Mechanochemistry of the alternatively spliced spectrin-actin binding domain in membrane skeletal protein 4.1. Discher, D.; Parra, M.; Conboy, J. G. Journal of Biological Chemistry, Vol. 268, Issue 10 https://doi.org/10.1016/S0021-9258(18)53163-X	journal	April 1993

Cited By (50)

Accurate and simultaneous identification of differential expression and splicing using hierarchical Bayesian analysis Karlebach, Guy; Hansen, Peter; Veiga, Diogo F. T. Genome Biology https://doi.org/10.1101/2019.12.16.878884	journal	December 2019
The changing paradigm of intron retention: regulation, ramifications and recipes Monteuuis, Geoffray; Wong, Justin J. L.; Bailey, Charles G. Nucleic Acids Research https://doi.org/10.1093/nar/gkz1068	journal	November 2019
Dynamic changes in intron retention are tightly associated with regulation of splicing factors and proliferative activity during B-cell development Ullrich, Sebastian; Guigó, Roderic Nucleic Acids Research, Vol. 48, Issue 3 https://doi.org/10.1093/nar/gkz1180	journal	December 2019
An Ultraconserved Element (UCE) controls homeostatic splicing of ARGLU1 mRNA Pirnie, Stephan P.; Osman, Ahmad; Zhu, Yinzhou Nucleic Acids Research, Vol. 45, Issue 6 https://doi.org/10.1093/nar/gkw1140	journal	November 2016
Widespread intronic polyadenylation diversifies immune cell transcriptomes Singh, Irtisha; Lee, Shih-Han; Sperling, Adam S. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04112-z	journal	April 2018
Sequences encoding C2H2 zinc fingers inhibit polyadenylation and mRNA export in human cells Russo, Joseph; Jalkanen, Aimee L.; Heck, Adam M. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-35138-4	journal	November 2018
The alternative splicing program of differentiated smooth muscle cells involves concerted non-productive splicing of post-transcriptional regulators Llorian, Miriam; Gooding, Clare; Bellora, Nicolas Nucleic Acids Research, Vol. 44, Issue 18 https://doi.org/10.1093/nar/gkw560	journal	June 2016
Predictive models of subcellular localization of long RNAs Zuckerman, Binyamin; Ulitsky, Igor RNA, Vol. 25, Issue 5 https://doi.org/10.1261/rna.068288.118	journal	February 2019
A dynamic intron retention program in the mammalian megakaryocyte and erythrocyte lineages Edwards, Christopher R.; Ritchie, William; Wong, Justin J. -L. Blood, Vol. 127, Issue 17 https://doi.org/10.1182/blood-2016-01-692764	journal	April 2016
We skip to work: alternative splicing in normal and malignant myelopoiesis Wong, Alex C. H.; Rasko, John E. J.; Wong, Justin J. -L. Leukemia, Vol. 32, Issue 5 https://doi.org/10.1038/s41375-018-0021-4	journal	January 2018
Spliceosomal gene mutations in myelodysplasia: molecular links to clonal abnormalities of hematopoiesis Inoue, Daichi; Bradley, Robert K.; Abdel-Wahab, Omar Genes & Development, Vol. 30, Issue 9 https://doi.org/10.1101/gad.278424.116	journal	May 2016
Intron Retention as a Mode for RNA-Seq Data Analysis Zheng, Jian-Tao; Lin, Cui-Xiang; Fang, Zhao-Yu Frontiers in Genetics, Vol. 11 https://doi.org/10.3389/fgene.2020.00586	journal	July 2020
HBA-DEALS: accurate and simultaneous identification of differential expression and splicing using hierarchical Bayesian analysis Karlebach, Guy; Hansen, Peter; Veiga, Diogo FT Genome Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s13059-020-02072-6	journal	July 2020
Comprehensive Proteomic Analysis of Human Erythropoiesis Gautier, Emilie-Fleur; Ducamp, Sarah; Leduc, Marjorie Cell Reports, Vol. 16, Issue 5 https://doi.org/10.1016/j.celrep.2016.06.085	journal	August 2016
Gene-centric functional dissection of human genetic variation uncovers regulators of hematopoiesis Nandakumar, Satish K.; McFarland, Sean K.; Mateyka, Laura M. eLife, Vol. 8 https://doi.org/10.7554/eLife.44080	journal	May 2019
Aberrant splicing and defective mRNA production induced by somatic spliceosome mutations in myelodysplasia Shiozawa, Yusuke; Malcovati, Luca; Gallì, Anna Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06063-x	journal	September 2018
SUPPA2: fast, accurate, and uncertainty-aware differential splicing analysis across multiple conditions Trincado, Juan L.; Entizne, Juan C.; Hysenaj, Gerald Genome Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s13059-018-1417-1	journal	March 2018
Epigenetic therapy of myelodysplastic syndromes connects to cellular differentiation independently of endogenous retroelement derepression. Kazachenka, Anastasiya; Young, George R.; Attig, Jan The Francis Crick Institute https://doi.org/10.25418/crick.11695179.v1	text	January 2020
Gene-Specific Intron Retention Serves as Molecular Signature that Distinguishes Melanoma from Non-Melanoma Cancer Cells in Greek Patients Giannopoulou, Aikaterini; Konstantakou, Eumorphia; Velentzas, Athanassios International Journal of Molecular Sciences, Vol. 20, Issue 4 https://doi.org/10.3390/ijms20040937	journal	February 2019
An atlas of alternative splicing profiles and functional associations reveals new regulatory programs and genes that simultaneously express multiple major isoforms Tapial, Javier; Ha, Kevin C. H.; Sterne-Weiler, Timothy Genome Research, Vol. 27, Issue 10 https://doi.org/10.1101/gr.220962.117	journal	August 2017
Nascent RNA and the Coordination of Splicing with Transcription Neugebauer, Karla M. Cold Spring Harbor Perspectives in Biology, Vol. 11, Issue 8 https://doi.org/10.1101/cshperspect.a032227	journal	August 2019
CLASS2: accurate and efficient splice variant annotation from RNA-seq reads Song, Li; Sabunciyan, Sarven; Florea, Liliana Nucleic Acids Research, Vol. 44, Issue 10 https://doi.org/10.1093/nar/gkw158	journal	March 2016
Co-regulatory activity of hnRNP K and NS1-BP in influenza and human mRNA splicing Thompson, Matthew G.; Muñoz-Moreno, Raquel; Bhat, Prasanna Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04779-4	journal	June 2018
Intron retention as a component of regulated gene expression programs Jacob, Aishwarya G.; Smith, Christopher W. J. Human Genetics, Vol. 136, Issue 9 https://doi.org/10.1007/s00439-017-1791-x	journal	April 2017
Increased intron retention is a post‐transcriptional signature associated with progressive aging and Alzheimer’s disease Adusumalli, Swarnaseetha; Ngian, Zhen‐Kai; Lin, Wei‐Qi Aging Cell, Vol. 18, Issue 3 https://doi.org/10.1111/acel.12928	journal	March 2019
Dynamic Transcriptional Landscape of the Early Chick Embryo Ren, Junxiao; Sun, Congjiao; Clinton, Michael Frontiers in Cell and Developmental Biology, Vol. 7 https://doi.org/10.3389/fcell.2019.00196	journal	September 2019
High Resolution Annotation of Zebrafish Transcriptome Using Long-Read Sequencing Nudelman, German; Frasca, Antonio; Kent, Brandon Genome Research https://doi.org/10.1101/174821	posted_content	August 2017
Global intron retention mediated gene regulation during CD4 ⁺ T cell activation Ni, Ting; Yang, Wenjing; Han, Miao Nucleic Acids Research, Vol. 44, Issue 14 https://doi.org/10.1093/nar/gkw591	journal	July 2016
Intron retention enhances gene regulatory complexity in vertebrates Schmitz, Ulf; Pinello, Natalia; Jia, Fangzhi Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1339-3	journal	November 2017
IntEREst: intron-exon retention estimator Oghabian, Ali; Greco, Dario; Frilander, Mikko J. BMC Bioinformatics, Vol. 19, Issue 1 https://doi.org/10.1186/s12859-018-2122-5	journal	April 2018
Alternative splicing as a regulator of development and tissue identity Baralle, Francisco E.; Giudice, Jimena Nature Reviews Molecular Cell Biology, Vol. 18, Issue 7 https://doi.org/10.1038/nrm.2017.27	journal	May 2017
A Conserved Splicing Silencer Dynamically Regulates O-GlcNAc Transferase Intron Retention and O-GlcNAc Homeostasis Park, Sung-Kyun; Zhou, Xiaorong; Pendleton, Kathryn E. Cell Reports, Vol. 20, Issue 5 https://doi.org/10.1016/j.celrep.2017.07.017	journal	August 2017
IRFinder: assessing the impact of intron retention on mammalian gene expression Middleton, Robert; Gao, Dadi; Thomas, Aubin Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1184-4	journal	March 2017
Alternative splicing analysis in human monocytes and macrophages reveals MBNL1 as major regulator Liu, Hongfei; Lorenzini, Paolo A.; Zhang, Fan Nucleic Acids Research, Vol. 46, Issue 12 https://doi.org/10.1093/nar/gky401	journal	May 2018
RNA-binding proteins in hematopoiesis and hematological malignancy Hodson, Daniel J.; Screen, Michael; Turner, Martin Blood, Vol. 133, Issue 22 https://doi.org/10.1182/blood-2018-10-839985	journal	May 2019
Glycogen synthase kinase-3 and alternative splicing Liu, Xiaolei; Klein, Peter S. Wiley Interdisciplinary Reviews: RNA, Vol. 9, Issue 6 https://doi.org/10.1002/wrna.1501	journal	August 2018
Timely-regulated intron retention as device to fine-tune protein expression Naro, Chiara; Sette, Claudio Cell Cycle, Vol. 16, Issue 14 https://doi.org/10.1080/15384101.2017.1337983	journal	June 2017
A Comprehensive Analysis of Alternative Splicing in Paleopolyploid Maize Mei, Wenbin; Liu, Sanzhen; Schnable, James C. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00694	journal	May 2017
Intron retention is regulated by altered MeCP2-mediated splicing factor recruitment Wong, Justin J. -L.; Gao, Dadi; Nguyen, Trung V. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15134	journal	May 2017
Intron retention is a source of neoepitopes in cancer Smart, Alicia C.; Margolis, Claire A.; Pimentel, Harold Nature Biotechnology, Vol. 36, Issue 11 https://doi.org/10.1038/nbt.4239	journal	August 2018
Nuclear sorting of RNA Garland, William; Jensen, Torben Heick WIREs RNA, Vol. 11, Issue 2 https://doi.org/10.1002/wrna.1572	journal	October 2019
Genome-wide analysis of alternative splicing events during response to drought stress in tomato ( Solanum lycopersicum L.) Lee, Hee Ju; Eom, Seung Hee; Lee, Jin Hyoung The Journal of Horticultural Science and Biotechnology https://doi.org/10.1080/14620316.2019.1656552	journal	August 2019
Intron retention as a component of regulated gene expression programs Jacob, Ag; Smith, Chris Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.11024	text	January 2017
RNA binding proteins in hematopoiesis and hematological malignancy. Hodson, Daniel; Screen, Michael; Turner, Martin Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.38967	text	January 2019
The alternative splicing program of differentiated smooth muscle cells involves concerted non-productive splicing of post-transcriptional regulators Llorian, Miriam; Gooding, Clare; Bellora, Nicolas Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.10731	text	January 2016
Post‐Transcriptional Noise Control Hansen, Maike M. K.; Weinberger, Leor S. BioEssays, Vol. 41, Issue 7 https://doi.org/10.1002/bies.201900044	journal	June 2019
High resolution annotation of zebrafish transcriptome using long-read sequencing Nudelman, German; Frasca, Antonio; Kent, Brandon Genome Research, Vol. 28, Issue 9 https://doi.org/10.1101/gr.223586.117	journal	July 2018
Epigenetic therapy of myelodysplastic syndromes connects to cellular differentiation independently of endogenous retroelement derepression Kazachenka, Anastasiya; Young, George R.; Attig, Jan Genome Medicine, Vol. 11, Issue 1 https://doi.org/10.1186/s13073-019-0707-x	journal	December 2019
Blood Relatives: Splicing Mechanisms underlying Erythropoiesis in Health and Disease Reimer, Kirsten A.; Neugebauer, Karla M. F1000Research, Vol. 7 https://doi.org/10.12688/f1000research.15442.1	journal	January 2018
Antisense Oligonucleotides Modulating Activation of a Nonsense-Mediated RNA Decay Switch Exon in the ATM Gene Kralovicova, Jana; Moreno, Pedro M. D.; Cross, Nicholas C. P. Nucleic Acid Therapeutics, Vol. 26, Issue 6 https://doi.org/10.1089/nat.2016.0635	journal	December 2016

Similar Records

An important class of intron retention events in human erythroblasts is regulated by cryptic exons proposed to function as splicing decoys

Journal Article · Fri Jun 29 00:00:00 EDT 2018 · RNA · OSTI ID:1256072

Parra, Marilyn; Booth, Ben W.; Weiszmann, Richard; +5 more

Antisense targeting of decoy exons can reduce intron retention and increase protein expression in human erythroblasts

Journal Article · Mon Apr 20 00:00:00 EDT 2020 · RNA · OSTI ID:1256072

Parra, Marilyn; Zhang, Weiguo; Vu, Jonathan; +2 more

A dynamic alternative splicing program regulates gene expression during terminal erythropoiesis

Journal Article · Fri Jan 17 00:00:00 EST 2014 · Nucleic Acids Research · OSTI ID:1256072

Pimentel, Harold; Parra, Marilyn; Gee, Sherry; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis

Citation Formats

References (48)

Cited By (50)

Similar Records

Related Subjects