Primary cilia control translation and the cell cycle in medulloblastoma

  1. Young-Goo Han1
  1. 1Department of Developmental Neurobiology, St. Jude Children's Research Hospital, Memphis, Tennessee 38105, USA;
  2. 2Department of Biochemistry and Cellular Biology, National Center of Neurology and Psychiatry, Tokyo 187-8551, Japan;
  3. 3Department of Pathology, St. Jude Children's Research Hospital, Memphis, Tennessee 38105, USA;
  4. 4Division of Neuro-Oncology, Department of Oncology, St. Jude Children's Research Hospital, Memphis, Tennessee 38105, USA;
  5. 5Department of Computational Biology, St. Jude Children's Research Hospital, Memphis, Tennessee 38105, USA;
  6. 6Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan;
  7. 7Department of Oncology, Cancer Research UK Cambridge Institute, Cambridge CB2 0RE, England;
  8. 8Department of Tumor Cell Biology, St. Jude Children's Research Hospital, Memphis, Tennessee 38105, USA
  1. Corresponding author: young-goo.han{at}stjude.org

Abstract

The primary cilium, a signaling organelle projecting from the surface of a cell, controls cellular physiology and behavior. The presence or absence of primary cilia is a distinctive feature of a given tumor type; however, whether and how the primary cilium contributes to tumorigenesis are unknown for most tumors. Medulloblastoma (MB) is a common pediatric brain cancer comprising four groups: SHH, WNT, group 3 (G3), and group 4 (G4). From 111 cases of MB, we show that primary cilia are abundant in SHH and WNT MBs but rare in G3 and G4 MBs. Using WNT and G3 MB mouse models, we show that primary cilia promote WNT MB by facilitating translation of mRNA encoding β-catenin, a major oncoprotein driving WNT MB, whereas cilium loss promotes G3 MB by disrupting cell cycle control and destabilizing the genome. Our findings reveal tumor type-specific ciliary functions and underlying molecular mechanisms. Moreover, we expand the function of primary cilia to translation control and reveal a molecular mechanism by which cilia regulate cell cycle progression, thereby providing new frameworks for studying cilium function in normal and pathologic conditions.

Keywords

Footnotes

  • Supplemental material is available for this article.

  • Article published online ahead of print. Article and publication date are online at http://www.genesdev.org/cgi/doi/10.1101/gad.349596.122.

  • Freely available online through the Genes & Development Open Access option.

  • Received March 24, 2022.
  • Accepted June 17, 2022.

This article, published in Genes & Development, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.

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