[en] Oncogenic protein dosage is tightly regulated to enable cancer formation but how this is regulated by translational control remains unknown. The Myc oncogene is a paradigm of an exquisitely regulated oncogene and a driver of pancreatic ductal adenocarcinoma (PDAC). Here we use a CRISPR interference screen in PDAC cells to identify activators of selective MYC translation. The top hit, the RNA-binding protein RBM42, is highly expressed in PDAC and predicts poor survival. We show that RBM42 binds and selectively regulates the translation of MYC and a precise suite of pro-oncogenic transcripts, including JUN and EGFR. Mechanistically, we find that RBM42 binds and remodels the MYC 5' untranslated region structure, facilitating the formation of the translation pre-initiation complex. Importantly, RBM42 is necessary for PDAC tumorigenesis in a Myc-dependent manner in vivo. This work transforms the understanding of the translational code in cancer and illuminates therapeutic openings to target the expression of oncogenes.
Disciplines :
Oncology
Author, co-author :
Kovalski, Joanna R ; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA
Sarioglu, Goksu ; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA
Subramanyam, Vishvak; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA ; Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, CA, USA
Hernandez, Grace; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA ; Department of Anatomy, University of California San Francisco, San Francisco, CA, USA ; Department of Pathology, University of California San Francisco, San Francisco, CA, USA
Rademaker, Gilles ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA ; Department of Anatomy, University of California San Francisco, San Francisco, CA, USA ; Department of Pathology, University of California San Francisco, San Francisco, CA, USA
Oses-Prieto, Juan A ; Department of Pharmaceutical Chemistry, University of California San Francisco, San Francisco, CA, USA
Slota, Macey ; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA
Mohan, Nimmy; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA
Yiakis, Kaylee; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA
Liu, Isabelle ; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA ; Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, CA, USA
Wen, Kwun Wah; Department of Pathology, University of California San Francisco, San Francisco, CA, USA
Kim, Grace E ; Department of Pathology, University of California San Francisco, San Francisco, CA, USA
Miglani, Sohit ; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA ; Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, CA, USA
Burlingame, Alma L; Department of Pharmaceutical Chemistry, University of California San Francisco, San Francisco, CA, USA
Goodarzi, Hani ; Department of Urology, University of California San Francisco, San Francisco, CA, USA ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA ; Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, CA, USA ; Arc Institute, Palo Alto, CA, USA
Perera, Rushika M ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA ; Department of Anatomy, University of California San Francisco, San Francisco, CA, USA ; Department of Pathology, University of California San Francisco, San Francisco, CA, USA
Ruggero, Davide ; Department of Urology, University of California San Francisco, San Francisco, CA, USA. davide.ruggero@ucsf.edu ; Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA. davide.ruggero@ucsf.edu ; Department of Cellular and Molecular Pharmacology, University of California San Francisco, San Francisco, CA, USA. davide.ruggero@ucsf.edu
Functional screen identifies RBM42 as a mediator of oncogenic mRNA translation specificity.
Publication date :
04 February 2025
Journal title :
Nature Cell Biology
ISSN :
1465-7392
eISSN :
1476-4679
Publisher :
Nature, England
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NIH. NCI - National Institutes of Health. National Cancer Institute ACS - American Cancer Society ACF - Association of Charitable Foundations
Funding text :
We thank all of the members of the Ruggero laboratory, especially D. Kuzuoglu-Öztürk, for critical discussion of the project and for manuscript feedback. We thank H. Karner (UCSF) for technical support for the CLIP experiments and B. Zarnegar (Stanford University) for CLIP advice and irCLIP reagents. Sequencing was performed at the UCSF CAT, supported by UCSF PBBR, RRP IMIA and NIH 1S10OD028511-01 grants. Fluorescence-activated cell sorting and BC43 spinning disk confocal microscopy were conducted in the HDFCCC Laboratory for Cell Analysis Shared Resource Facility through a grant from NIH (P30CA082103). Mass spectrometry was provided by the Mass Spectrometry Resource at UCSF (A. L. Burlingame, Director), supported by the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation. J.R.K. was funded by an American Cancer Society postdoctoral fellowship (133966‐PF‐20‐009‐01‐RMC) and a UCSF Mentored Scientist Award in Pancreas Cancer (RAP 7031426). G.H. was supported by the National Science Foundation Graduate Research Fellowship Program (NSF2034836). H.G. is an Arc Institute Core Investigator. Research in the H.G. laboratory is supported by the Arc Institute. R.M.P. is funded by R01CA240603 (NCI; NIH), an AACR-MPM Oncology Charitable Foundation Transformative Cancer Research Grant and an Ed Marra Passion to Win Fund. D.R. is funded by the NIH (R35CA242986) and the American Cancer Society (American Cancer Society Research Professor Award). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
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