Structural basis underlying CAC RNA recognition by the RRM domain of dimeric RNA-binding protein RBPMS

Teplova, Marianna; Farazi, Thalia A.; Tuschl, Thomas; Patel, Dinshaw J.

doi:10.1017/S0033583515000207

Title: Structural basis underlying CAC RNA recognition by the RRM domain of dimeric RNA-binding protein RBPMS

Journal Article · Tue Sep 08 00:00:00 EDT 2015 · Quarterly Reviews of Biophysics

DOI:https://doi.org/10.1017/S0033583515000207· OSTI ID:1430282

Teplova, Marianna ^[1]; Farazi, Thalia A. ^[2]; Tuschl, Thomas ^[2]; Patel, Dinshaw J. ^[1]

Memorial Sloan-Kettering Cancer Center, New York, NY (United States)
The Rockefeller Univ., New York, NY (United States)

RNA-binding protein with multiple splicing (designated RBPMS) is a higher vertebrate mRNA-binding protein containing a single RNA recognition motif (RRM). RBPMS has been shown to be involved in mRNA transport, localization and stability, with key roles in axon guidance, smooth muscle plasticity, as well as regulation of cancer cell proliferation and migration. We report on structure-function studies of the RRM domain of RBPMS bound to a CAC-containing single-stranded RNA. These results provide insights into potential topologies of complexes formed by the RBPMS RRM domain and the tandem CAC repeat binding sites as detected by photoactivatable-ribonucleoside-enhanced crosslinking and immunoprecipitation. These studies establish that the RRM domain of RBPMS forms a symmetrical dimer in the free state, with each monomer binding sequence-specifically to all three nucleotides of a CAC segment in the RNA bound state. Structure-guided mutations within the dimerization and RNA-binding interfaces of RBPMS RRM on RNA complex formation resulted in both disruption of dimerization and a decrease in RNA-binding affinity as observed by size exclusion chromatography and isothermal titration calorimetry. Here, as anticipated from biochemical binding studies, over-expression of dimerization or RNA-binding mutants of Flag-HA-tagged RBPMS were no longer able to track with stress granules in HEK293 cells, thereby documenting the deleterious effects of such mutations in vivo.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH); RU CCTS

Grant/Contract Number:: R01GM104962; UL1RR024143

OSTI ID:: 1430282

Journal Information:: Quarterly Reviews of Biophysics, Vol. 49, Issue 2016; ISSN 0033-5835

Publisher:: Cambridge University PressCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 22 works

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Exploring the Activities of RBPMS Proteins in Myocardial Biology Akerberg, Alexander A.; Burns, Caroline E.; Burns, C. Geoffrey Pediatric Cardiology, Vol. 40, Issue 7 https://doi.org/10.1007/s00246-019-02180-6	journal	August 2019
Accuracy and precision of protein structures determined by magic angle spinning NMR spectroscopy: for some ‘with a little help from a friend’ Russell, Ryan W.; Fritz, Matthew P.; Kraus, Jodi Journal of Biomolecular NMR, Vol. 73, Issue 6-7 https://doi.org/10.1007/s10858-019-00233-9	journal	March 2019
Molecular basis for AU-rich element recognition and dimerization by the HuR C-terminal RRM Ripin, Nina; Boudet, Julien; Duszczyk, Malgorzata M. Proceedings of the National Academy of Sciences, Vol. 116, Issue 8 https://doi.org/10.1073/pnas.1808696116	journal	February 2019
Exploring the molecular basis of RNA recognition by the dimeric RNA-binding protein via molecular simulation methods Chang, Shan; Zhang, Da-Wei; Xu, Lei RNA Biology, Vol. 13, Issue 11 https://doi.org/10.1080/15476286.2016.1223007	journal	September 2016
Identification of RBPMS as a smooth muscle master splicing regulator via proximity of its gene with super-enhancers Nakagaki-Silva, Erick E.; Gooding, Clare; Llorian, Miriam eLife https://doi.org/10.1101/563304	journal	March 2019
Expanding the spectrum of pediatric NTRK ‐rearranged fibroblastic tumors to the central nervous system: A case report with RBPMS‐NTRK3 fusion Torre, Matthew; Jessop, Nicholas; Hornick, Jason L. Neuropathology, Vol. 38, Issue 6 https://doi.org/10.1111/neup.12513	journal	September 2018
rbpms2 functions in Balbiani body architecture and ovary fate Kaufman, Odelya H.; Lee, KathyAnn; Martin, Manon PLOS Genetics, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pgen.1007489	journal	July 2018
Identification of RBPMS as a mammalian smooth muscle master splicing regulator via proximity of its gene with super-enhancers Nakagaki-Silva, Erick E.; Gooding, Clare; Llorian, Miriam eLife, Vol. 8 https://doi.org/10.7554/elife.46327	journal	July 2019
Crystal structure of human Acinus RNA recognition motif domain Fernandes, Humberto; Czapinska, Honorata; Grudziaz, Katarzyna PeerJ, Vol. 6 https://doi.org/10.7717/peerj.5163	journal	January 2018
Identification of RBPMS as a mammalian smooth muscle master splicing regulator via proximity of its gene with super-enhancers. Nakagaki-Silva, Erick E.; Gooding, Clare; Llorian, Miriam Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.41008	text	January 2019
Molecular basis for AU-rich element recognition and dimerization by the HuR C-terminal RRM Nina, Ripin,; Julien, Boudet,; M., Duszczyk, Malgorzata ETH Zurich https://doi.org/10.3929/ethz-b-000328390	text	January 2019

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Title: Structural basis underlying CAC RNA recognition by the RRM domain of dimeric RNA-binding protein RBPMS

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