Identification of the RNA Recognition Element of the RBPMS Family of RNA-binding Proteins and Their Transcriptome-wide MRNA Targets

Overview

Journal RNA

Specialty Molecular Biology

Date 2014 May 27

PMID 24860013

Citations 32

Authors

Thalia A Farazi

Carl S Leonhardt

Neelanjan Mukherjee

Aleksandra Mihailovic

Song Li

Klaas E A Max

Cindy Meyer

Masashi Yamaji

Pavol cekan

Nicholas C Jacobs

Stefanie Gerstberger

Claudia Bognanni

Erik Larsson

Uwe Ohler

Thomas Tuschl

Affiliations

Soon will be listed here.

Abstract

Recent studies implicated the RNA-binding protein with multiple splicing (RBPMS) family of proteins in oocyte, retinal ganglion cell, heart, and gastrointestinal smooth muscle development. These RNA-binding proteins contain a single RNA recognition motif (RRM), and their targets and molecular function have not yet been identified. We defined transcriptome-wide RNA targets using photoactivatable-ribonucleoside-enhanced crosslinking and immunoprecipitation (PAR-CLIP) in HEK293 cells, revealing exonic mature and intronic pre-mRNA binding sites, in agreement with the nuclear and cytoplasmic localization of the proteins. Computational and biochemical approaches defined the RNA recognition element (RRE) as a tandem CAC trinucleotide motif separated by a variable spacer region. Similar to other mRNA-binding proteins, RBPMS family of proteins relocalized to cytoplasmic stress granules under oxidative stress conditions suggestive of a support function for mRNA localization in large and/or multinucleated cells where it is preferentially expressed.

Citing Articles

The RNA-binding protein RBPMS inhibits smooth muscle cell-driven vascular remodeling in atherosclerosis and vascular injury.

Du J, Yuan X, Wang J, Zhang L, Tan F, Hu T Proc Natl Acad Sci U S A. 2025; 122(9):e2415933122.

PMID: 39999164 PMC: 11892686. DOI: 10.1073/pnas.2415933122.

RNA binding protein with multiple splicing (RBPMS) promotes contractile phenotype splicing in human embryonic stem cell-derived vascular smooth muscle cells.

Jacob A, Moutsopoulos I, Petchey A, Kollyfas R, Knight-Schrijver V, Mohorianu I Cardiovasc Res. 2024; 120(16):2104-2116.

PMID: 39248180 PMC: 11646123. DOI: 10.1093/cvr/cvae198.

RNA binding proteins in cardiovascular development and disease.

Verma S, Kuyumcu-Martinez M Curr Top Dev Biol. 2024; 156:51-119.

PMID: 38556427 PMC: 11896630. DOI: 10.1016/bs.ctdb.2024.01.007.

Rbpms2 promotes female fate upstream of the nutrient sensing Gator2 complex component, Mios.

Wilson M, Romano S, Khatri N, Aharon D, Liu Y, Kaufman O bioRxiv. 2024; .

PMID: 38328218 PMC: 10849709. DOI: 10.1101/2024.01.25.577235.

SH3RF2 contributes to cisplatin resistance in ovarian cancer cells by promoting RBPMS degradation.

Gong T, Liu F, Xiao Q, Li Y, Wei Y, Xu H Commun Biol. 2024; 7(1):67.

PMID: 38195842 PMC: 10776562. DOI: 10.1038/s42003-023-05721-1.

References

Defrance M, Janky R, Sand O, van Helden J . Using RSAT oligo-analysis and dyad-analysis tools to discover regulatory signals in nucleic sequences. Nat Protoc. 2008; 3(10):1589-603. DOI: 10.1038/nprot.2008.98. View

Hui J, Stangl K, Lane W, Bindereif A . HnRNP L stimulates splicing of the eNOS gene by binding to variable-length CA repeats. Nat Struct Biol. 2002; 10(1):33-7. DOI: 10.1038/nsb875. View

Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov J . GenePattern 2.0. Nat Genet. 2006; 38(5):500-1. DOI: 10.1038/ng0506-500. View

Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley D . Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012; 7(3):562-78. PMC: 3334321. DOI: 10.1038/nprot.2012.016. View

Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H . The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012; 22(9):1775-89. PMC: 3431493. DOI: 10.1101/gr.132159.111. View

Spitzer J, Landthaler M, Tuschl T . Rapid creation of stable mammalian cell lines for regulated expression of proteins using the Gateway® recombination cloning technology and Flp-In T-REx® lines. Methods Enzymol. 2013; 529:99-124. DOI: 10.1016/B978-0-12-418687-3.00008-2. View

Kubalak S, Miller-Hance W, OBrien T, Dyson E, Chien K . Chamber specification of atrial myosin light chain-2 expression precedes septation during murine cardiogenesis. J Biol Chem. 1994; 269(24):16961-70. View

Wang X, Tanaka Hall T . Structural basis for recognition of AU-rich element RNA by the HuD protein. Nat Struct Biol. 2001; 8(2):141-5. DOI: 10.1038/84131. View

Trapnell C, Pachter L, Salzberg S . TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25(9):1105-11. PMC: 2672628. DOI: 10.1093/bioinformatics/btp120. View

10.

Kwong J, Caprioli J, Piri N . RNA binding protein with multiple splicing: a new marker for retinal ganglion cells. Invest Ophthalmol Vis Sci. 2009; 51(2):1052-8. PMC: 3979483. DOI: 10.1167/iovs.09-4098. View

11.

. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 2011; 9(4):e1001046. PMC: 3079585. DOI: 10.1371/journal.pbio.1001046. View

12.

Song H, Cauffman K, Chan A, Zhou Y, King M, Etkin L . Hermes RNA-binding protein targets RNAs-encoding proteins involved in meiotic maturation, early cleavage, and germline development. Differentiation. 2007; 75(6):519-28. DOI: 10.1111/j.1432-0436.2006.00155.x. View

13.

Oubridge C, Ito N, Evans P, Teo C, Nagai K . Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature. 1994; 372(6505):432-8. DOI: 10.1038/372432a0. View

14.

Lebedeva S, Jens M, Theil K, Schwanhausser B, Selbach M, Landthaler M . Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell. 2011; 43(3):340-52. DOI: 10.1016/j.molcel.2011.06.008. View

15.

Buchan J, Parker R . Eukaryotic stress granules: the ins and outs of translation. Mol Cell. 2010; 36(6):932-41. PMC: 2813218. DOI: 10.1016/j.molcel.2009.11.020. View

16.

Mukherjee N, Corcoran D, Nusbaum J, Reid D, Georgiev S, Hafner M . Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell. 2011; 43(3):327-39. PMC: 3220597. DOI: 10.1016/j.molcel.2011.06.007. View

17.

Betley J, Heinrich B, Vernos I, Sardet C, Prodon F, Deshler J . Kinesin II mediates Vg1 mRNA transport in Xenopus oocytes. Curr Biol. 2004; 14(3):219-24. DOI: 10.1016/j.cub.2004.01.028. View

18.

Kwon S, Yi H, Eichelbaum K, Fohr S, Fischer B, You K . The RNA-binding protein repertoire of embryonic stem cells. Nat Struct Mol Biol. 2013; 20(9):1122-30. DOI: 10.1038/nsmb.2638. View

19.

Miller B, Stamatoyannopoulos J . Integrative meta-analysis of differential gene expression in acute myeloid leukemia. PLoS One. 2010; 5(3):e9466. PMC: 2830886. DOI: 10.1371/journal.pone.0009466. View

20.

Larsson E, Lindahl P, Mostad P . HeliCis: a DNA motif discovery tool for colocalized motif pairs with periodic spacing. BMC Bioinformatics. 2007; 8:418. PMC: 2200674. DOI: 10.1186/1471-2105-8-418. View