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

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 developmentallydynamic 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 nuclearlocalized. 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. Finally, 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)

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1256072

Alternate ID(s):: OSTI ID: 1379053

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

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Additional file 2 of Coordinated changes in gene expression kinetics underlie both mouse and human erythroid maturation Barile, Melania; Imaz-Rosshandler, Ivan; Inzani, Isabella figshare https://doi.org/10.6084/m9.figshare.14913222.v1	dataset	January 2021
Additional file 3 of Coordinated changes in gene expression kinetics underlie both mouse and human erythroid maturation Barile, Melania; Imaz-Rosshandler, Ivan; Inzani, Isabella figshare https://doi.org/10.6084/m9.figshare.14913225	dataset	January 2021
Additional file 4 of Coordinated changes in gene expression kinetics underlie both mouse and human erythroid maturation Barile, Melania; Imaz-Rosshandler, Ivan; Inzani, Isabella figshare https://doi.org/10.6084/m9.figshare.14913228.v1	dataset	January 2021
Additional file 6 of Coordinated changes in gene expression kinetics underlie both mouse and human erythroid maturation Barile, Melania; Imaz-Rosshandler, Ivan; Inzani, Isabella figshare https://doi.org/10.6084/m9.figshare.14913234	dataset	January 2021
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