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Coordination of alternative splicing and alternative polyadenylation revealed by targeted long read sequencing

Author

Listed:
  • Zhiping Zhang

    (University of Connecticut School of Medicine
    University of Nevada, Reno)

  • Bongmin Bae

    (University of Nevada, Reno)

  • Winston H. Cuddleston

    (University of Nevada, Reno)

  • Pedro Miura

    (University of Connecticut School of Medicine
    University of Nevada, Reno
    University of Connecticut)

Abstract

Nervous system development is associated with extensive regulation of alternative splicing (AS) and alternative polyadenylation (APA). AS and APA have been extensively studied in isolation, but little is known about how these processes are coordinated. Here, the coordination of cassette exon (CE) splicing and APA in Drosophila was investigated using a targeted long-read sequencing approach we call Pull-a-Long-Seq (PL-Seq). This cost-effective method uses cDNA pulldown and Nanopore sequencing combined with an analysis pipeline to quantify inclusion of alternative exons in connection with alternative 3’ ends. Using PL-Seq, we identified genes that exhibit significant differences in CE splicing depending on connectivity to short versus long 3’UTRs. Genomic long 3’UTR deletion was found to alter upstream CE splicing in short 3’UTR isoforms and ELAV loss differentially affected CE splicing depending on connectivity to alternative 3’UTRs. This work highlights the importance of considering connectivity to alternative 3’UTRs when monitoring AS events.

Suggested Citation

  • Zhiping Zhang & Bongmin Bae & Winston H. Cuddleston & Pedro Miura, 2023. "Coordination of alternative splicing and alternative polyadenylation revealed by targeted long read sequencing," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41207-8
    DOI: 10.1038/s41467-023-41207-8
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    1. Brenton R. Graveley & Angela N. Brooks & Joseph W. Carlson & Michael O. Duff & Jane M. Landolin & Li Yang & Carlo G. Artieri & Marijke J. van Baren & Nathan Boley & Benjamin W. Booth & James B. Brown , 2011. "The developmental transcriptome of Drosophila melanogaster," Nature, Nature, vol. 471(7339), pages 473-479, March.
    2. Eric T. Wang & Rickard Sandberg & Shujun Luo & Irina Khrebtukova & Lu Zhang & Christine Mayr & Stephen F. Kingsmore & Gary P. Schroth & Christopher B. Burge, 2008. "Alternative isoform regulation in human tissue transcriptomes," Nature, Nature, vol. 456(7221), pages 470-476, November.
    3. Gloria M. Sheynkman & Katharine S. Tuttle & Florent Laval & Elizabeth Tseng & Jason G. Underwood & Liang Yu & Da Dong & Melissa L. Smith & Robert Sebra & Luc Willems & Tong Hao & Michael A. Calderwood, 2020. "ORF Capture-Seq as a versatile method for targeted identification of full-length isoforms," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    4. Herve Rhinn & Liang Qiang & Toru Yamashita & David Rhee & Ari Zolin & William Vanti & Asa Abeliovich, 2012. "Alternative α-synuclein transcript usage as a convergent mechanism in Parkinson's disease pathology," Nature Communications, Nature, vol. 3(1), pages 1-11, January.
    5. Ya Cui & Frederick J. Arnold & Fanglue Peng & Dan Wang & Jason Sheng Li & Sebastian Michels & Eric J. Wagner & Albert R. Spada & Wei Li, 2023. "Alternative polyadenylation transcriptome-wide association study identifies APA-linked susceptibility genes in brain disorders," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Mandeep Singh & Ghamdan Al-Eryani & Shaun Carswell & James M. Ferguson & James Blackburn & Kirston Barton & Daniel Roden & Fabio Luciani & Tri Giang Phan & Simon Junankar & Katherine Jackson & Christo, 2019. "High-throughput targeted long-read single cell sequencing reveals the clonal and transcriptional landscape of lymphocytes," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    7. James B. Brown & Nathan Boley & Robert Eisman & Gemma E. May & Marcus H. Stoiber & Michael O. Duff & Ben W. Booth & Jiayu Wen & Soo Park & Ana Maria Suzuki & Kenneth H. Wan & Charles Yu & Dayu Zhang &, 2014. "Diversity and dynamics of the Drosophila transcriptome," Nature, Nature, vol. 512(7515), pages 393-399, August.
    8. Donny D. Licatalosi & Aldo Mele & John J. Fak & Jernej Ule & Melis Kayikci & Sung Wook Chi & Tyson A. Clark & Anthony C. Schweitzer & John E. Blume & Xuning Wang & Jennifer C. Darnell & Robert B. Darn, 2008. "HITS-CLIP yields genome-wide insights into brain alternative RNA processing," Nature, Nature, vol. 456(7221), pages 464-469, November.
    9. Chioniso P. Masamha & Zheng Xia & Jingxuan Yang & Todd R. Albrecht & Min Li & Ann-Bin Shyu & Wei Li & Eric J. Wagner, 2014. "CFIm25 links alternative polyadenylation to glioblastoma tumour suppression," Nature, Nature, vol. 510(7505), pages 412-416, June.
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