Online citations, reference lists, and bibliographies.

The Minor And Major Spliceosome Interact To Regulate Alternative Splicing Around Minor Introns

Anouk M. Olthof, Alisa K. White, Madisen F. Lee, Almahdi Chakroun, Alice K. Abdel Aleem, Justine Rousseau, C. Magnani, Philippe M. Campeau, Rahul N. Kanadia
Published 2020 · Biology
Cite This
Download PDF
Analyze on Scholarcy
Share
Mutations in minor spliceosome components are linked to diseases such as Roifman syndrome, Lowry-Wood syndrome, and early-onset cerebellar ataxia (EOCA). Here we report that besides increased minor intron retention, Roifman syndrome and EOCA can also be characterized by elevated alternative splicing (AS) around minor introns. Consistent with the idea that the assembly/activity of the minor spliceosome informs AS in minor intron-containing genes (MIGs), inhibition of all minor spliceosome snRNAs led to upregulated AS. Notably, alternatively spliced MIG isoforms were bound to polysomes in the U11-null dorsal telencephalon, which suggested that aberrant MIG protein expression could contribute to disease pathogenesis. In agreement, expression of an aberrant isoform of the MIG Dctn3 by in utero electroporation, affected radial glial cell divisions. Finally, we show that AS around minor introns is executed by the major spliceosome and is regulated by U11-59K of the minor spliceosome, which forms exon-bridging interactions with proteins of the major spliceosome. Overall, we extend the exon-definition model to MIGs and postulate that disruptions of exon-bridging interactions might contribute to disease severity and pathogenesis.
This paper references
10.1038/ncomms9718
Compound heterozygous mutations in the noncoding RNU4ATAC cause Roifman Syndrome by disrupting minor intron splicing
Daniele Merico (2015)
10.1093/nar/27.6.1524
Characterization of a novel mouse cDNA, ES18, involved in apoptotic cell death of T-cells.
E. Park (1999)
10.1016/0092-8674(88)90509-0
A factor, U2AF, is required for U2 snRNP binding and splicing complex assembly
B. Ruskin (1988)
10.4324/9781315131771-7
Loss of Will
Oacar Handlin (2017)
10.1126/science.1202205
Association of TALS Developmental Disorder with Defect in Minor Splicing Component U4atac snRNA
P. Edery (2011)
10.1101/gad.6.12b.2554
U1 snRNP targets an essential splicing factor, U2AF65, to the 3' splice site by a network of interactions spanning the exon.
Bob Hoffman (1992)
10.1126/science.274.5289.1005
U1-Mediated Exon Definition Interactions Between AT-AC and GT-AG Introns
Q. Wu (1996)
10.1093/nar/gkr1056
Functional mammalian spliceosomal complex E contains SMN complex proteins in addition to U1 and U2 snRNPs
Evgeny M. Makarov (2012)
10.1186/s12864-019-6046-x
Minor intron splicing revisited: identification of new minor intron-containing genes and tissue-dependent retention and alternative splicing of minor introns
Anouk M. Olthof (2019)
10.1002/ajmg.a.38581
The expanding phenotype of RNU4ATAC pathogenic variants to Lowry Wood syndrome.
Laura S Farach (2018)
Citron Kinase Affects a Subset of Progenitor Cells That Alters Late but Not Early Neurogenesis in the Developing Rat RetinaRole of Citron Kinase in Retinal Neurogenesis
The many pathways of RNA
J Houseley (2009)
10.3389/fgene.2019.01113
An Integrated Model of Minor Intron Emergence and Conservation
Marybeth Baumgartner (2019)
10.1016/j.ijdevneu.2006.09.022
The cell biology of neurogenesis
W. Huttner (2006)
10.1016/j.semcdb.2017.09.036
Minor spliceosome and disease.
Bhupendra Verma (2018)
10.1101/gad.1974810
The U2AF35-related protein Urp contacts the 3' splice site to promote U12-type intron splicing and the second step of U2-type intron splicing.
Haihong Shen (2010)
10.1074/jbc.M400270200
Interactions of Arabidopsis RS Domain Containing Cyclophilins with SR Proteins and U1 and U11 Small Nuclear Ribonucleoprotein-specific Proteins Suggest Their Involvement in Pre-mRNA Splicing*
Z. Lorković (2004)
10.1016/S0092-8674(00)81057-0
A Novel Spliceosome Containing U11, U12, and U5 snRNPs Excises a Minor Class (AT–AC) Intron In Vitro
W. Tarn (1996)
10.1093/nar/23.16.3260
U1 snRNP-ASF/SF2 interaction and 5' splice site recognition: characterization of required elements.
S. Jamison (1995)
10.7554/eLife.33178
ICE1 promotes the link between splicing and nonsense-mediated mRNA decay
Thomas D Baird (2018)
10.1073/pnas.1305536111
Minor class splicing shapes the zebrafish transcriptome during development
Sebastian J. Markmiller (2014)
10.1083/jcb.201208098
Systematic dissection of dynein regulators in mitosis
Jonne A Raaijmakers (2013)
10.1002/ana.24826
Mutation in noncoding RNA RNU12 causes early onset cerebellar ataxia
Mahmoud F. Elsaid (2017)
10.1073/pnas.0604970103
Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy.
Rahul N. Kanadia (2006)
10.15252/embj.201593791
Minor intron splicing is regulated by FUS and affected by ALS-associated FUS mutants.
S. Reber (2016)
10.1038/nrg2402
The multiple lives of NMD factors: balancing roles in gene and genome regulation
O. Isken (2008)
10.1093/nar/gkv468
ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap
Tauno Metsalu (2015)
10.1038/nature05228
An early evolutionary origin for the minor spliceosome
A. Russell (2006)
10.1002/art.24586
Anti-U11/U12 RNP antibodies in systemic sclerosis: a new serologic marker associated with pulmonary fibrosis.
Noreen Fertig (2009)
10.1101/pdb.prot073650
piggyBac transposon-mediated cellular transgenesis in mammalian forebrain by in utero electroporation.
Fuyi Chen (2014)
10.1002/wrna.1140
Exon and intron definition in pre-mRNA splicing.
Laura de Conti (2013)
10.1016/j.molcel.2010.02.014
An ancient mechanism for splicing control: U11 snRNP as an activator of alternative splicing.
Jens Verbeeren (2010)
10.1128/MCB.10.1.84
Exon definition may facilitate splice site selection in RNAs with multiple exons.
B. Robberson (1990)
10.1261/rna.7320604
The human 18S U11/U12 snRNP contains a set of novel proteins not found in the U2-dependent spliceosome.
C. Will (2004)
10.1093/nar/gkn923
Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists
Da Wei Huang (2009)
10.1073/pnas.0608484103
ELYS is a dual nucleoporin/kinetochore protein required for nuclear pore assembly and proper cell division
B. Rasala (2006)
10.1093/nar/gkf609
Domains of human U4atac snRNA required for U12-dependent splicing in vivo.
G. Shukla (2002)
10.1186/1471-2164-15-S8-S2
Bootstrap-based differential gene expression analysis for RNA-Seq data with and without replicates
Sahar Al Seesi (2014)
10.1093/nar/gni041
Targeted ‘knockdown’ of spliceosome function in mammalian cells
Nathalie Matter (2005)
10.1101/gad.294769.116
Targeting RNA for processing or destruction by the eukaryotic RNA exosome and its cofactors.
John C. Zinder (2017)
10.1038/ncomms7042
Aberrant splicing of U12-type introns is the hallmark of ZRSR2 mutant myelodysplastic syndrome
Vikas Madan (2015)
10.1007/s00439-018-1950-8
Lowry-Wood syndrome: further evidence of association with RNU4ATAC, and correlation between genotype and phenotype
Ivan Shelihan (2018)
10.1101/gr.849004
WebLogo: a sequence logo generator.
G. Crooks (2004)
10.1002/ijc.31638
miR-134 targets PDCD7 to reduce E-cadherin expression and enhance oral cancer progression.
Shih-Yuan Peng (2018)
10.14785/LYMPHOSIGN-2016-0015
A novel mutation in Roifman syndrome redefines the boundaries of the Sm protein-binding site
Yael Dinur-Schejter (2016)
10.1002/emmm.201303573
Defective minor spliceosome mRNA processing results in isolated familial growth hormone deficiency
Jesús Argente (2014)
10.1126/science.1200587
Mutations in U4atac snRNA, a Component of the Minor Spliceosome, in the Developmental Disorder MOPD I
Huiling He (2011)
10.1242/dev.166322
Minor spliceosome inactivation causes microcephaly, owing to cell cycle defects and death of self-amplifying radial glial cells
Marybeth Baumgartner (2018)
10.1126/science.273.5283.1824
Highly Diverged U4 and U6 Small Nuclear RNAs Required for Splicing Rare AT-AC Introns
W. Tarn (1996)
10.1128/MCB.00424-06
Cortical Migration Defects in Mice Expressing A-RAF from the B-RAF Locus
Guadalupe Camarero (2006)
10.1186/1471-2164-15-S9-S2
TINAGL1 and B3GALNT1 are potential therapy target genes to suppress metastasis in non-small cell lung cancer
H. Umeyama (2014)
10.1016/0092-8674(93)90316-I
Specific interactions between proteins implicated in splice site selection and regulated alternative splicing
J. Wu (1993)
10.1091/mbc.E09-05-0377
The Nup107-160 nucleoporin complex promotes mitotic events via control of the localization state of the chromosome passenger complex.
Melpomeni Platani (2009)
10.1093/bioinformatics/btx365
Fast bootstrapping‐based estimation of confidence intervals of expression levels and differential expression from RNA‐Seq data
Igor Mandric (2017)
10.1126/science.284.5422.2003
Identification of both shared and distinct proteins in the major and minor spliceosomes.
Cindy L Will (1999)
10.1261/rna.071423.119
New insights into minor splicing - A transcriptomic analysis of cells derived from TALS patients.
Audric Cologne (2019)
10.1523/JNEUROSCI.22-15-06309.2002
Cortical Excitatory Neurons and Glia, But Not GABAergic Neurons, Are Produced in the Emx1-Expressing Lineage
J. Gorski (2002)
10.1093/nar/gkv1344
The Pfam protein families database: towards a more sustainable future
R. Finn (2016)
10.1038/nbt.1511
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification
J. Cox (2008)
10.1002/ajmg.a.32773
Multiple joint dislocations: an additional skeletal finding in Lowry-Wood syndrome?
Cinzia Magnani (2009)
Universal sample preparation method for proteome analysis
Claire E Eyers (2009)
10.1002/wrna.1141
The significant other: splicing by the minor spliceosome
Janne J. Turunen (2013)
10.1167/iovs.14-15272
Loss of citron kinase affects a subset of progenitor cells that alters late but not early neurogenesis in the developing rat retina.
Devi Krishna Priya Karunakaran (2015)
10.1016/j.cub.2003.12.058
The Vertebrate Ndc80 Complex Contains Spc24 and Spc25 Homologs, which Are Required to Establish and Maintain Kinetochore-Microtubule Attachment
M. McCleland (2004)
10.1146/annurev.biochem.76.050106.093909
The nonsense-mediated decay RNA surveillance pathway.
Yao-Fu Chang (2007)
10.1073/pnas.0907143106
Cell-type-specific isolation of ribosome-associated mRNA from complex tissues
Elisenda Sanz (2009)
10.7554/eLife.00780
Minor introns are embedded molecular switches regulated by highly unstable U6atac snRNA
Ihab Younis (2013)
10.1016/j.cell.2009.01.019
The Many Pathways of RNA Degradation
Jonathan Houseley (2009)
10.1105/tpc.020743
Determinants of Plant U12-Dependent Intron Splicing Efficiency
D. Lewandowska (2004)
10.1093/bioinformatics/btq033
BEDTools: a flexible suite of utilities for comparing genomic features
Aaron R. Quinlan (2010)
10.1038/nmeth.3317
HISAT: a fast spliced aligner with low memory requirements
Daehwan Kim (2015)



Semantic Scholar Logo Some data provided by SemanticScholar