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In silico RNA isoform screening to identify potential cancer driver exons with therapeutic applications

Author

Listed:
  • Miquel Anglada-Girotto

    (Dr. Aiguader 88)

  • Ludovica Ciampi

    (Dr. Aiguader 88)

  • Sophie Bonnal

    (Dr. Aiguader 88)

  • Sarah A. Head

    (Dr. Aiguader 88)

  • Samuel Miravet-Verde

    (Dr. Aiguader 88
    ETH Zurich)

  • Luis Serrano

    (Dr. Aiguader 88
    Universitat Pompeu Fabra (UPF)
    Pg. Lluís Companys 23)

Abstract

Alternative splicing is crucial for cancer progression and can be targeted pharmacologically, yet identifying driver exons genome-wide remains challenging. We propose identifying such exons by associating statistically gene-level cancer dependencies from knockdown viability screens with splicing profiles and gene expression. Our models predict the effects of splicing perturbations on cell proliferation from transcriptomic data, enabling in silico RNA screening and prioritizing targets for splicing-based therapies. We identified 1,073 exons impacting cell proliferation, many from genes not previously linked to cancer. Experimental validation confirms their influence on proliferation, especially in highly proliferative cancer cell lines. Integrating pharmacological screens with splicing dependencies highlights the potential driver exons affecting drug sensitivity. Our models also allow predicting treatment outcomes from tumor transcriptomes, suggesting applications in precision oncology. This study presents an approach to identifying cancer driver exon and their therapeutic potential, emphasizing alternative splicing as a cancer target.

Suggested Citation

  • Miquel Anglada-Girotto & Ludovica Ciampi & Sophie Bonnal & Sarah A. Head & Samuel Miravet-Verde & Luis Serrano, 2024. "In silico RNA isoform screening to identify potential cancer driver exons with therapeutic applications," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51380-z
    DOI: 10.1038/s41467-024-51380-z
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    as
    1. James M. McFarland & Zandra V. Ho & Guillaume Kugener & Joshua M. Dempster & Phillip G. Montgomery & Jordan G. Bryan & John M. Krill-Burger & Thomas M. Green & Francisca Vazquez & Jesse S. Boehm & Tod, 2018. "Improved estimation of cancer dependencies from large-scale RNAi screens using model-based normalization and data integration," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    2. Wei-Ching Chen & Minh D. To & Peter M. K. Westcott & Reyno Delrosario & Il-Jin Kim & Mark Philips & Quan Tran & Saumya R. Bollam & Hani Goodarzi & Nora Bayani & Olga Mirzoeva & Allan Balmain, 2021. "Targeting KRAS4A splicing through the RBM39/DCAF15 pathway inhibits cancer stem cells," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Tongsen Zheng & Jiabei Wang & Yuhan Zhao & Cen Zhang & Meihua Lin & Xiaowen Wang & Haiyang Yu & Lianxin Liu & Zhaohui Feng & Wenwei Hu, 2013. "Spliced MDM2 isoforms promote mutant p53 accumulation and gain-of-function in tumorigenesis," Nature Communications, Nature, vol. 4(1), pages 1-12, December.
    4. W. Frank Lenoir & Micaela Morgado & Peter C. DeWeirdt & Megan McLaughlin & Audrey L. Griffith & Annabel K. Sangree & Marissa N. Feeley & Nazanin Esmaeili Anvar & Eiru Kim & Lori L. Bertolet & Medina C, 2021. "Discovery of putative tumor suppressors from CRISPR screens reveals rewired lipid metabolism in acute myeloid leukemia cells," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    5. Nadezhda V. Terekhanova & Alla Karpova & Wen-Wei Liang & Alexander Strzalkowski & Siqi Chen & Yize Li & Austin N. Southard-Smith & Michael D. Iglesia & Michael C. Wendl & Reyka G. Jayasinghe & Jingxia, 2023. "Epigenetic regulation during cancer transitions across 11 tumour types," Nature, Nature, vol. 623(7986), pages 432-441, November.
    6. Eric L. Nostrand & Peter Freese & Gabriel A. Pratt & Xiaofeng Wang & Xintao Wei & Rui Xiao & Steven M. Blue & Jia-Yu Chen & Neal A. L. Cody & Daniel Dominguez & Sara Olson & Balaji Sundararaman & Liju, 2020. "A large-scale binding and functional map of human RNA-binding proteins," Nature, Nature, vol. 583(7818), pages 711-719, July.
    7. Debashish Ray & Hilal Kazan & Kate B. Cook & Matthew T. Weirauch & Hamed S. Najafabadi & Xiao Li & Serge Gueroussov & Mihai Albu & Hong Zheng & Ally Yang & Hong Na & Manuel Irimia & Leah H. Matzat & R, 2013. "A compendium of RNA-binding motifs for decoding gene regulation," Nature, Nature, vol. 499(7457), pages 172-177, July.
    8. Mahmoud Ghandi & Franklin W. Huang & Judit Jané-Valbuena & Gregory V. Kryukov & Christopher C. Lo & E. Robert McDonald & Jordi Barretina & Ellen T. Gelfand & Craig M. Bielski & Haoxin Li & Kevin Hu & , 2019. "Next-generation characterization of the Cancer Cell Line Encyclopedia," Nature, Nature, vol. 569(7757), pages 503-508, May.
    Full references (including those not matched with items on IDEAS)

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