Home LiteratureArticle Details
PMID: 33975916 Published · aheadofprint English Journal Article

Co-transcriptional splicing efficiencies differ within genes and between cell types.

RNA (New York, N.Y.) ·2021-05-11

Bedi K, Magnuson BR, Narayanan I, Paulsen M, Wilson TE, Ljungman M

Abstract

Pre-mRNA splicing is carried out by the spliceosome and involves splice site recognition, removal of introns, and ligation of exons. Components of the spliceosome have been shown to interact with the elongating RNA polymerase II (RNAPII) which is thought to allow splicing to occur concurrently with transcription. However, little is known about the regulation and efficiency of co-transcriptional splicing in human cells. In this study, we used Bru-seq and BruChase-seq to determine the co-transcriptional splicing efficiencies of 17,000 introns expressed across 6 human cell lines. We found that less than half of all introns across these 6 cell lines were co-transcriptionally spliced. Splicing efficiencies for individual introns showed variations across cell lines, suggesting that splicing may be regulated in a cell-type specific manner. Moreover, the splicing efficiency of introns varied within genes. The efficiency of co-transcriptional splicing did not correlate with gene length, intron position, splice site strengths, or the intron/neighboring exons GC content. However, we identified binding signals from multiple RNA binding proteins (RBPs) that correlated with splicing efficiency, including core spliceosomal machinery components-such as SF3B4, U2AF1 and U2AF2 showing higher binding signals in poorly spliced introns. In addition, multiple RBPs, such as BUD13, PUM1 and SND1, showed preferential binding in exons that flank introns with high splicing efficiencies. The nascent RNA splicing patterns presented here across multiple cell types add to our understanding of the complexity in RNA splicing, wherein RNA-binding proteins may play important roles in determining splicing outcomes in a cell type- and intron-specific manner.

Keywords
RNA binding proteins cell lines cotranscriptional spliceosome splicing
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Bedi Karan ORCID
University of Michigan.
Magnuson Brian R ORCID
University of Michigan.
Narayanan Ishwarya ORCID
University of Michigan.
Paulsen Michelle
University of Michigan.
Wilson Thomas E ORCID
University of Michigan.
Ljungman Mats ORCID
University of Michigan [email protected].
References (74)
74 references, click to expand
  1. A genome-wide analysis indicates that yeast pre-mRNA splicing is predominantly posttranscriptional.
    Mol Cell. 2006 Dec 28;24(6):917-29 PMID: 17189193
  2. Structures of human Pumilio with noncognate RNAs reveal molecular mechanisms for binding promiscuity.
    Structure. 2008 Apr;16(4):549-57 PMID: 18328718
  3. Principles of RNA processing from analysis of enhanced CLIP maps for 150 RNA binding proteins.
    Genome Biol. 2020 Apr 6;21(1):90 PMID: 32252787
  4. Ultrashort and progressive 4sU-tagging reveals key characteristics of RNA processing at nucleotide resolution.
    Genome Res. 2012 Oct;22(10):2031-42 PMID: 22539649
  5. Sorting out the complexity of SR protein functions.
    RNA. 2000 Sep;6(9):1197-211 PMID: 10999598
  6. Coupling mRNA processing with transcription in time and space.
    Nat Rev Genet. 2014 Mar;15(3):163-75 PMID: 24514444
  7. Co-transcriptional splicing of constitutive and alternative exons.
    RNA. 2009 Oct;15(10):1896-908 PMID: 19656867
  8. Nucleosome positioning as a determinant of exon recognition.
    Nat Struct Mol Biol. 2009 Sep;16(9):996-1001 PMID: 19684599
  9. Alternative RNA structures formed during transcription depend on elongation rate and modify RNA processing.
    Mol Cell. 2021 Apr 15;81(8):1789-1801.e5 PMID: 33631106
  10. deepTools2: a next generation web server for deep-sequencing data analysis.
    Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5 PMID: 27079975
  11. Co-transcriptional splicing regulates 3' end cleavage during mammalian erythropoiesis.
    Mol Cell. 2021 Mar 4;81(5):998-1012.e7 PMID: 33440169
  12. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.
    Nat Biotechnol. 2010 May;28(5):511-5 PMID: 20436464
  13. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals.
    J Comput Biol. 2004;11(2-3):377-94 PMID: 15285897
  14. Pre-mRNA splicing is facilitated by an optimal RNA polymerase II elongation rate.
    Genes Dev. 2014 Dec 1;28(23):2663-76 PMID: 25452276
  15. A splicing-dependent transcriptional checkpoint associated with prespliceosome formation.
    Mol Cell. 2014 Mar 6;53(5):779-90 PMID: 24560925
  16. Splicing Kinetics and Coordination Revealed by Direct Nascent RNA Sequencing through Nanopores.
    Mol Cell. 2020 Mar 5;77(5):985-998.e8 PMID: 31839405
  17. Detained introns are a novel, widespread class of post-transcriptionally spliced introns.
    Genes Dev. 2015 Jan 1;29(1):63-80 PMID: 25561496
  18. 4sUDRB-seq: measuring genomewide transcriptional elongation rates and initiation frequencies within cells.
    Genome Biol. 2014 May 09;15(5):R69 PMID: 24887486
  19. Widespread intron retention in mammals functionally tunes transcriptomes.
    Genome Res. 2014 Nov;24(11):1774-86 PMID: 25258385
  20. An extensive network of coupling among gene expression machines.
    Nature. 2002 Apr 4;416(6880):499-506 PMID: 11932736
  21. Coordinated regulation of synthesis and stability of RNA during the acute TNF-induced proinflammatory response.
    Proc Natl Acad Sci U S A. 2013 Feb 5;110(6):2240-5 PMID: 23345452
  22. Mechanisms of alternative pre-messenger RNA splicing.
    Annu Rev Biochem. 2003;72:291-336 PMID: 12626338
  23. Genome-wide association between branch point properties and alternative splicing.
    PLoS Comput Biol. 2010 Nov 24;6(11):e1001016 PMID: 21124863
  24. Tudor-SN-mediated endonucleolytic decay of human cell microRNAs promotes G1/S phase transition.
    Science. 2017 May 26;356(6340):859-862 PMID: 28546213
  25. Rate of elongation by RNA polymerase II is associated with specific gene features and epigenetic modifications.
    Genome Res. 2014 Jun;24(6):896-905 PMID: 24714810
  26. Landscape of transcription in human cells.
    Nature. 2012 Sep 6;489(7414):101-8 PMID: 22955620
  27. The yeast RNA gene products are essential for mRNA splicing in vitro.
    Cell. 1986 Dec 26;47(6):953-63 PMID: 3536128
  28. Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila.
    Genes Dev. 2011 Dec 1;25(23):2502-12 PMID: 22156210
  29. Rates of in situ transcription and splicing in large human genes.
    Nat Struct Mol Biol. 2009 Nov;16(11):1128-33 PMID: 19820712
  30. The G-quartet containing FMRP binding site in FMR1 mRNA is a potent exonic splicing enhancer.
    Nucleic Acids Res. 2008 Sep;36(15):4902-12 PMID: 18653529
  31. The in vivo kinetics of RNA polymerase II elongation during co-transcriptional splicing.
    PLoS Biol. 2011 Jan 11;9(1):e1000573 PMID: 21264352
  32. A universal code for RNA recognition by PUF proteins.
    Nat Chem Biol. 2011 May 15;7(7):425-7 PMID: 21572425
  33. Post-transcriptional splicing of nascent RNA contributes to widespread intron retention in plants.
    Nat Plants. 2020 Jul;6(7):780-788 PMID: 32541953
  34. Cloning and domain structure of the mammalian splicing factor U2AF.
    Nature. 1992 Feb 13;355(6361):609-14 PMID: 1538748
  35. Comprehensive splice-site analysis using comparative genomics.
    Nucleic Acids Res. 2006;34(14):3955-67 PMID: 16914448
  36. Cloning and characterization of human DDX24 and mouse Ddx24, two novel putative DEAD-Box proteins, and mapping DDX24 to human chromosome 14q32.
    Genomics. 2000 Aug 1;67(3):351-5 PMID: 10936056
  37. POINT technology illuminates the processing of polymerase-associated intact nascent transcripts.
    Mol Cell. 2021 May 6;81(9):1935-1950.e6 PMID: 33735606
  38. Structure of the human activated spliceosome in three conformational states.
    Cell Res. 2018 Mar;28(3):307-322 PMID: 29360106
  39. Mammalian NET-Seq Reveals Genome-wide Nascent Transcription Coupled to RNA Processing.
    Cell. 2015 Apr 23;161(3):526-540 PMID: 25910207
  40. Long-read sequencing of nascent RNA reveals coupling among RNA processing events.
    Genome Res. 2018 Jul;28(7):1008-1019 PMID: 29903723
  41. Splicing of yeast nuclear pre-mRNA in vitro requires a functional 40S spliceosome and several extrinsic factors.
    Genes Dev. 1987 Mar;1(1):7-18 PMID: 3322937
  42. Chromatin organization marks exon-intron structure.
    Nat Struct Mol Biol. 2009 Sep;16(9):990-5 PMID: 19684600
  43. Deep sequencing of subcellular RNA fractions shows splicing to be predominantly co-transcriptional in the human genome but inefficient for lncRNAs.
    Genome Res. 2012 Sep;22(9):1616-25 PMID: 22955974
  44. A new regulatory protein, KSRP, mediates exon inclusion through an intronic splicing enhancer.
    Genes Dev. 1997 Apr 15;11(8):1023-36 PMID: 9136930
  45. Specific and modular binding code for cytosine recognition in Pumilio/FBF (PUF) RNA-binding domains.
    J Biol Chem. 2011 Jul 29;286(30):26732-42 PMID: 21653694
  46. Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing.
    Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4325-30 PMID: 19251664
  47. Fast gapped-read alignment with Bowtie 2.
    Nat Methods. 2012 Mar 04;9(4):357-9 PMID: 22388286
  48. Independent mechanisms recruit the cohesin loader protein NIPBL to sites of DNA damage.
    J Cell Sci. 2017 Mar 15;130(6):1134-1146 PMID: 28167679
  49. STAR: ultrafast universal RNA-seq aligner.
    Bioinformatics. 2013 Jan 1;29(1):15-21 PMID: 23104886
  50. TT-seq maps the human transient transcriptome.
    Science. 2016 Jun 3;352(6290):1225-8 PMID: 27257258
  51. Spliceosome assembly is coupled to RNA polymerase II dynamics at the 3' end of human genes.
    Nat Struct Mol Biol. 2011 Sep 04;18(10):1115-23 PMID: 21892168
  52. GENCODE reference annotation for the human and mouse genomes.
    Nucleic Acids Res. 2019 Jan 8;47(D1):D766-D773 PMID: 30357393
  53. Pre-mRNA splicing and human disease.
    Genes Dev. 2003 Feb 15;17(4):419-37 PMID: 12600935
  54. Cotranscriptional splicing efficiency differs dramatically between Drosophila and mouse.
    RNA. 2012 Dec;18(12):2174-86 PMID: 23097425
  55. A slow RNA polymerase II affects alternative splicing in vivo.
    Mol Cell. 2003 Aug;12(2):525-32 PMID: 14536091
  56. Evidence that the human homologue of a rat initiation factor-2 associated protein (p67) is a methionine aminopeptidase.
    Biochem Biophys Res Commun. 1996 Oct 3;227(1):152-9 PMID: 8858118
  57. Use of Bru-Seq and BruChase-Seq for genome-wide assessment of the synthesis and stability of RNA.
    Methods. 2014 May 1;67(1):45-54 PMID: 23973811
  58. Improving RNA-Seq expression estimates by correcting for fragment bias.
    Genome Biol. 2011;12(3):R22 PMID: 21410973
  59. Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions.
    Cell. 2012 Jul 20;150(2):279-90 PMID: 22817891
  60. Conservation of structure and subunit interactions in yeast homologues of splicing factor 3b (SF3b) subunits.
    RNA. 1998 Jan;4(1):1-10 PMID: 9436903
  61. Splice site selection, rate of splicing, and alternative splicing on nascent transcripts.
    Genes Dev. 1988 Jun;2(6):754-65 PMID: 3138163
  62. Identification of cis-acting elements and splicing factors involved in the regulation of BIM Pre-mRNA splicing.
    PLoS One. 2014 Apr 17;9(4):e95210 PMID: 24743263
  63. The "spliceosome": yeast pre-messenger RNA associates with a 40S complex in a splicing-dependent reaction.
    Science. 1985 May 24;228(4702):963-7 PMID: 3890181
  64. Regulation of alternative splicing through coupling with transcription and chromatin structure.
    Annu Rev Biochem. 2015;84:165-98 PMID: 26034889
  65. A general role for splicing enhancers in exon definition.
    RNA. 2002 Oct;8(10):1233-41 PMID: 12403462
  66. Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons.
    Elife. 2014 Apr 29;3:e02407 PMID: 24843027
  67. Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases.
    Trends Biochem Sci. 2000 Mar;25(3):106-10 PMID: 10694877
  68. Counting on co-transcriptional splicing.
    F1000Prime Rep. 2013 Apr 02;5:9 PMID: 23638305
  69. Coupling and coordination in gene expression processes with pre-mRNA splicing.
    Int J Mol Sci. 2015 Mar 11;16(3):5682-96 PMID: 25768347
  70. Splicing of Nascent RNA Coincides with Intron Exit from RNA Polymerase II.
    Cell. 2016 Apr 7;165(2):372-381 PMID: 27020755
  71. From structure to systems: high-resolution, quantitative genetic analysis of RNA polymerase II.
    Cell. 2013 Aug 15;154(4):775-88 PMID: 23932120
  72. Splicing of Balbiani ring 1 gene pre-mRNA occurs simultaneously with transcription.
    Cell. 1994 Jan 14;76(1):183-92 PMID: 8287477
  73. Reflections on the history of pre-mRNA processing and highlights of current knowledge: a unified picture.
    RNA. 2013 Apr;19(4):443-60 PMID: 23440351
  74. Total RNA sequencing reveals nascent transcription and widespread co-transcriptional splicing in the human brain.
    Nat Struct Mol Biol. 2011 Nov 06;18(12):1435-40 PMID: 22056773
Full Text / Full Text
PMC full text available locally, click to read

Loading full text...

Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1469-9001
Published
2021-05-11
Epub
2021-00-11
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC8208053
Subset
IM
Grants
NCI NIH HHS · R01 CA213214 · United States
NHGRI NIH HHS · UM1 HG009382 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]