Global analysis of RNA-binding protein dynamics by comparative and enhanced RNA interactome capture

Joel I. Perez-Perri, Marko Noerenberg, Wael Kamel, Caroline E. Lenz, Shabaz Mohammed, Matthias W. Hentze, Alfredo Castello

Published: 2020-11-17 DOI: 10.1038/s41596-020-00404-1

Proteomics

RNA-binding proteins

RNA interactome capture

Locked Nucleic Acid

SILAC and TMT

AI 解读

Efficient and safe single-cell cloning of human pluripotent stem cells using the CEPT cocktail

Profiling native pulmonary basement membrane stiffness using atomic force microscopy

Genetic circuit design automation with Cello 2.0

Synthesis of siRNA nanoparticles to silence plaque-destabilizing gene in atherosclerotic lesional macrophages

Scalable dual-omics profiling with single-nucleus chromatin accessibility and mRNA expression sequencing 2 (SNARE-seq2)

A practical guide to scanning light-field microscopy with digital adaptive optics

Effective high-throughput isolation of fully human antibodies targeting infectious pathogens

Improved sampling and DNA extraction procedures for microbiome analysis in food-processing environments

MOF-derived nanoporous carbons with diverse tunable nanoarchitectures

Tutorial: a statistical genetics guide to identifying HLA alleles driving complex disease

查看全部

Sections

Figures

References

Interactions between RNA-binding proteins (RBPs) and RNAs are critical to cell biology. However, methods to comprehensively and quantitatively assess these interactions within cells were lacking. RNA interactome capture (RIC) uses invivo UV crosslinking,
Introduction
Materials
Procedure
Troubleshooting
Timing
Anticipated results
References
ACKNOWLEDGMENTS
ACKNOWLEDGMENTS

Urdaneta, E. C. et al. Purification of cross-linked RNA-protein complexes by phenol-toluol extraction. Nat. Commun. 10, 990 (2019).
Burger, K. et al. 4-thiouridine inhibits rRNA synthesis and causes a nucleolar stress response. RNA Biol. 10, 1623–1630 (2013).
Muckenthaler, M. U., Rivella, S., Hentze, M. W. & Galy, B. A red carpet for iron metabolism. Cell 168, 344–361 (2017).
Altelaar, A. F. et al. Benchmarking stable isotope labeling based quantitative proteomics. J. Proteomics 88, 14–26 (2013).
Baltz, A. G. et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol. Cell 46, 674–690 (2012).
Castello, A. et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149, 1393–1406 (2012).
Castello, A. et al. System-wide identification of RNA-binding proteins by interactome capture. Nat. Protoc. 8, 491–500 (2013).
Kwon, S. C. et al. The RNA-binding protein repertoire of embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1122–1130 (2013).
Beckmann, B. M. et al. The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs. Nat. Commun. 6, 10127 (2015).
Liao, Y. et al. The cardiomyocyte RNA-binding proteome: links to intermediary metabolism and heart disease. Cell Rep. 16, 1456–1469 (2016).
Liepelt, A. et al. Identification of RNA-binding proteins in macrophages by interactome capture. Mol Cell Proteomics 15, 2699–2714 (2016).
Matia-Gonzalez, A. M., Laing, E. E. & Gerber, A. P. Conserved mRNA-binding proteomes in eukaryotic organisms. Nat. Struct. Mol. Biol. 22, 1027–1033 (2015).
Reichel, M. et al. In planta determination of the mRNA-binding proteome of Arabidopsis etiolated seedlings. Plant Cell 28, 2435–2452 (2016).
Sysoev, V. O. et al. Global changes of the RNA-bound proteome during the maternal-to-zygotic transition in Drosophila. Nat. Commun. 7, 12128 (2016).
Despic, V. et al. Dynamic RNA-protein interactions underlie the zebrafish maternal-to-zygotic transition. Genome Res. 27, 1184–1194 (2017).
Nandan, D. et al. Comprehensive identification of mRNA-binding proteins of Leishmania donovani by interactome capture. PLoS ONE 12, e0170068 (2017).
Bach-Pages, M. et al. Discovering the RNA-binding proteome of plant leaves with an improved rna interactome capture method. Biomolecules 10, 661 (2020).
Perez-Perri, J. I. et al. Discovery of RNA-binding proteins and characterization of their dynamic responses by enhanced RNA interactome capture. Nat. Commun. 9, 4408 (2018).
Garcia-Moreno, M. et al. System-wide profiling of RNA-binding proteins uncovers key regulators of virus infection. Mol. Cell 74, 196–211 e111 (2019).
Rogell, B. et al. Specific RNP capture with antisense LNA/DNA mixmers. RNA 23, 1290–1302 (2017).
Ong, S. E. & Mann, M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 1, 2650–2660 (2006).
Hughes, C. S. et al. Ultrasensitive proteome analysis using paramagnetic bead technology. Mol. Syst. Biol. 10, 757 (2014).
Hughes, C. S. et al. Single-pot, solid-phase-enhanced sample preparation for proteomics experiments. Nat. Protoc. 14, 68–85 (2019).
Lukong, K. E., Chang, K. W., Khandjian, E. W. & Richard, S. RNA-binding proteins in human genetic disease. Trends Genet. 24, 416–425 (2008).
Castello, A., Fischer, B., Hentze, M. W. & Preiss, T. RNA-binding proteins in Mendelian disease. Trends Genet. 29, 318–327 (2013).
Moore, S., Jarvelin, A. I., Davis, I., Bond, G. L. & Castello, A. Expanding horizons: new roles for non-canonical RNA-binding proteins in cancer. Curr. Opin. Genet. Dev. 48, 112–120 (2018).
Garcia-Moreno, M., Jarvelin, A. I. & Castello, A. Unconventional RNA-binding proteins step into the virus-host battlefront. Wiley Interdiscip. Rev. RNA 9, e1498 (2018).
Castello, A., Hentze, M. W. & Preiss, T. Metabolic enzymes enjoying new partnerships as RNA-binding proteins. Trends Endocrinol. Metab. 26, 746–757 (2015).
Hentze, M. W., Castello, A., Schwarzl, T. & Preiss, T. A brave new world of RNA-binding proteins. Nat. Rev. Mol. Cell Biol. 19, 327–341 (2018).
Horos, R. et al. The small non-coding vault RNA1-1 acts as a riboregulator of autophagy. Cell 176, 1054–1067 e1012 (2019).
Choudhury, N. R. et al. RNA-binding activity of TRIM25 is mediated by its PRY/SPRY domain and is required for ubiquitination. BMC Biol. 15, 105 (2017).
Jiao, A. L. & Slack, F. J. RNA-mediated gene activation. Epigenetics 9, 27–36 (2014).
Ivanyi-Nagy, R. et al. The RNA interactome of human telomerase RNA reveals a coding-independent role for a histone mRNA in telomere homeostasis. eLife http://doi.org/10.7554/eLife.40037 (2018).
Kumari, P. & Sampath, K. cncRNAs: bi-functional RNAs with protein coding and non-coding functions. Semin. Cell Dev. Biol. 47-48, 40–51 (2015).
Castello, A. et al. Comprehensive identification of RNA-binding domains in human cells. Mol. Cell 63, 696–710 (2016).
Castello, A. et al. Identification of RNA-binding domains of RNA-binding proteins in cultured cells on a system-wide scale with RBDmap. Nat. Protoc. 12, 2447–2464 (2017).
Backlund, M. et al. Plasticity of nuclear and cytoplasmic stress responses of RNA-binding proteins. Nucleic Acids Res. 48, 4725–4740 (2020).
Bunnik, E. M. et al. The mRNA-bound proteome of the human malaria parasite Plasmodium falciparum. Genome Biol. 17, 147 (2016).
Wessels, H. H. et al. The mRNA-bound proteome of the early fly embryo. Genome Res. 26, 1000–1009 (2016).
Kilchert, C. et al. System-wide analyses of the fission yeast poly(A)(+) RNA interactome reveal insights into organization and function of RNA-protein complexes. Genome Res. http://doi.org/10.1101/gr.257006.119 (2020).
Bao, X. et al. Capturing the interactome of newly transcribed RNA. Nat. Methods 15, 213–220 (2018).
Huang, R., Han, M., Meng, L. & Chen, X. Capture and identification of RNA-binding proteins by using click chemistry-assisted RNA-interactome capture (CARIC) strategy. J Vis. Exp. http://doi.org/10.3791/58580 (2018).
Asencio, C., Chatterjee, A. & Hentze, M. W. Silica-based solid-phase extraction of cross-linked nucleic acid-bound proteins. Life Sci. Alliance 1, e201800088 (2018).
Shchepachev, V. et al. Defining the RNA interactome by total RNA-associated protein purification. Mol. Syst. Biol. 15, e8689 (2019).
Trendel, J. et al. The human RNA-binding proteome and its dynamics during translational arrest. Cell 176, 391–403 e319 (2019).
Queiroz, R. M. L. et al. Comprehensive identification of RNA-protein interactions in any organism using orthogonal organic phase separation (OOPS). Nat. Biotechnol. 37, 169–178 (2019).
Hogrebe, A. et al. Benchmarking common quantification strategies for large-scale phosphoproteomics. Nat. Commun. 9, 1045 (2018).
Dimayacyac-Esleta, B. R. et al. Rapid high-pH reverse phase StageTip for sensitive small-scale membrane proteomic profiling. Anal. Chem. 87, 12016–12023 (2015).
Greenberg, J. R. Ultraviolet light-induced crosslinking of mRNA to proteins. Nucleic Acids Res. 6, 715–732 (1979).
He, C. et al. High-resolution mapping of RNA-Binding regions in the nuclear proteome of embryonic stem cells. Mol. Cell 64, 416–430 (2016).
Wisniewski, J. R., Zougman, A., Nagaraj, N. & Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods 6, 359–362 (2009).
Niu, L. et al. Modified TCA/acetone precipitation of plant proteins for proteomic analysis. PLoS ONE 13, e0202238 (2018).
Sielaff, M. et al. Evaluation of FASP, SP3, and iST protocols for proteomic sample preparation in the low microgram range. J. Proteome Res. 16, 4060–4072 (2017).
Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896–1906 (2007).
Villen, J. & Gygi, S. P. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat. Protoc. 3, 1630–1638 (2008).
Krijgsveld, J., Gauci, S., Dormeyer, W. & Heck, A. J. In-gel isoelectric focusing of peptides as a tool for improved protein identification. J. Proteome Res. 5, 1721–1730 (2006).
Tyanova, S., Temu, T. & Cox, J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat. Protoc. 11, 2301–2319 (2016).
Gierlinski, M., Gastaldello, F., Cole, C. & Barton, G. J. Proteus: an R package for downstream analysis of MaxQuant output. Preprint at bioRxiv http://doi.org/10.1101/416511 (2018).
Lazar, C., Gatto, L., Ferro, M., Bruley, C. & Burger, T. Accounting for the multiple natures of missing values in label-free quantitative proteomics data sets to compare imputation strategies. J. Proteome Res. 15, 1116–1125 (2016).
Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794–1805 (2011).
Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
Harsha, H. C., Molina, H. & Pandey, A. Quantitative proteomics using stable isotope labeling with amino acids in cell culture. Nat. Protoc. 3, 505–516 (2008).
Anantharaman, V. & Aravind, L. The PRC-barrel: a widespread, conserved domain shared by photosynthetic reaction center subunits and proteins of RNA metabolism. Genome Biol. 3, RESEARCH0061 (2002).
Dennis, G. Jr. et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3 (2003).
Strein, C., Alleaume, A. M., Rothbauer, U., Hentze, M. W. & Castello, A. A versatile assay for RNA-binding proteins in living cells. RNA 20, 721–731 (2014).
Konig, J. et al. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat. Struct. Mol. Biol. 17, 909–915 (2010).
Hafner, M. et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129–141 (2010).
Van Nostrand, E. L. et al. Robust transcriptome-wide discovery of RNA-binding protein binding sites with enhanced CLIP (eCLIP). Nat. Methods 13, 508–514 (2016).
Van Nostrand, E. L. et al. A large-scale binding and functional map of human RNA-binding proteins. Nature 583, 711–719 (2020).
Jarvelin, A. I., Noerenberg, M., Davis, I. & Castello, A. The new (dis)order in RNA regulation. Cell Commun. Signal 14, 9 (2016).
Arif, A. et al. The GAIT translational control system. Wiley Interdiscip. Rev. RNA http://doi.org/10.1002/wrna.1441 (2018).

Global analysis of RNA-binding protein dynamics by comparative and enhanced RNA interactome capture

Supplementary information

Supplementary Information

Reporting Summary

Supplementary Software

推荐阅读