A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis
Abstract
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.
- Authors:
-
- 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
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1256072
- Alternate Identifier(s):
- OSTI ID: 1379053
- Grant/Contract Number:
- AC02-05CH1123; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 44; Journal Issue: 2; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Pimentel, Harold, Parra, Marilyn, Gee, Sherry L., Mohandas, Narla, Pachter, Lior, and Conboy, John G. A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis. United States: N. p., 2015.
Web. doi:10.1093/nar/gkv1168.
Pimentel, Harold, Parra, Marilyn, Gee, Sherry L., Mohandas, Narla, Pachter, Lior, & Conboy, John G. A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis. United States. https://doi.org/10.1093/nar/gkv1168
Pimentel, Harold, Parra, Marilyn, Gee, Sherry L., Mohandas, Narla, Pachter, Lior, and Conboy, John G. Tue .
"A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis". United States. https://doi.org/10.1093/nar/gkv1168. https://www.osti.gov/servlets/purl/1256072.
@article{osti_1256072,
title = {A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis},
author = {Pimentel, Harold and Parra, Marilyn and Gee, Sherry L. and Mohandas, Narla and Pachter, Lior and Conboy, John G.},
abstractNote = {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.},
doi = {10.1093/nar/gkv1168},
journal = {Nucleic Acids Research},
number = 2,
volume = 44,
place = {United States},
year = {Tue Nov 03 00:00:00 EST 2015},
month = {Tue Nov 03 00:00:00 EST 2015}
}
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