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New Insights into the RNA-Binding and E3 Ubiquitin Ligase Activities of Roquins.

Zhang Q, Fan L, Hou F, Dong A, Wang YX, Tong Y
Sci Rep 5 15660 (2015)
Cited: 17 times
EuropePMC logo PMID: 26489670

Abstract

Roquins are a family of highly conserved RNA-binding proteins that also contain a RING-type E3 ubiquitin ligase domain. They repress constitutive decay elements containing mRNAs and play a critical role in RNA homeostasis and immunological self-tolerance. Here we present the crystal structures of the RNA-binding region of Roquin paralog RC3H2 in both apo- and RNA-bound forms. The RNA-binding region has a bipartite architecture composed of ROQ and HEPN domains, and can bind to stem-loop and double-stranded RNAs simultaneously. The two domains undergo a large orientation change to accommodate RNA duplex binding. We profiled E2 ubiquitin-conjugating enzymes that pair with Roquins and found that RC3H1 and RC3H2 interact with two sets of overlapping but not identical E2 enzymes to drive the assembly of polyubiquitin chains of different linkages. Crystal structures, small-angle X-ray scattering, and E2 profiling revealed that while the two paralogs are highly homologous, RC3H2 and RC3H1 are different in their structures and functions. We also demonstrated that RNA duplex binding to RC3H2 cross-talks with its E3 ubiquitin ligase function using an in vitro auto-ubiquitination assay.

Reviews citing this publication (7)

  1. Ubiquitin signaling in immune responses. Hu H, Sun SC. Cell Res 26 457-483 (2016)
  2. RNA-binding proteins in immune regulation: a focus on CCCH zinc finger proteins. Fu M, Blackshear PJ. Nat Rev Immunol 17 130-143 (2017)
  3. Recent insights of T cell receptor-mediated signaling pathways for T cell activation and development. Hwang JR, Byeon Y, Kim D, Park SG. Exp Mol Med 52 750-761 (2020)
  4. RNA-binding proteins control gene expression and cell fate in the immune system. Turner M, Díaz-Muñoz MD. Nat Immunol 19 120-129 (2018)
  5. Regulation of mRNA stability by CCCH-type zinc-finger proteins in immune cells. Maeda K, Akira S. Int Immunol 29 149-155 (2017)
  6. ROQUIN signalling pathways in innate and adaptive immunity. Athanasopoulos V, Ramiscal RR, Vinuesa CG. Eur J Immunol 46 1082-1090 (2016)
  7. ZC3H12A/MCPIP1/Regnase-1-related endonucleases: An evolutionary perspective on molecular mechanisms and biological functions. Habacher C, Ciosk R. Bioessays 39 (2017)

Articles citing this publication (10)

  1. A CAF40-binding motif facilitates recruitment of the CCR4-NOT complex to mRNAs targeted by Drosophila Roquin. Sgromo A, Raisch T, Bawankar P, Bhandari D, Chen Y, Kuzuoğlu-Öztürk D, Weichenrieder O, Izaurralde E. Nat Commun 8 14307 (2017)
  2. Functional insights from a surface antigen mRNA-bound proteome. Melo do Nascimento L, Egler F, Arnold K, Papavasiliou N, Clayton C, Erben E. Elife 10 e68136 (2021)
  3. Interaction profiling of RNA-binding ubiquitin ligases reveals a link between posttranscriptional regulation and the ubiquitin system. Hildebrandt A, Alanis-Lobato G, Voigt A, Zarnack K, Andrade-Navarro MA, Beli P, König J. Sci Rep 7 16582 (2017)
  4. Deiminated proteins in extracellular vesicles and serum of llama (Lama glama)-Novel insights into camelid immunity. Criscitiello MF, Kraev I, Lange S. Mol Immunol 117 37-53 (2020)
  5. Identification of new high affinity targets for Roquin based on structural conservation. Braun J, Fischer S, Xu ZZ, Sun H, Ghoneim DH, Gimbel AT, Plessmann U, Urlaub H, Mathews DH, Weigand JE. Nucleic Acids Res 46 12109-12125 (2018)
  6. RNA-Binding RING E3-Ligase DZIP3/hRUL138 Stabilizes Cyclin D1 to Drive Cell-Cycle and Cancer Progression. Kolapalli SP, Sahu R, Chauhan NR, Jena KK, Mehto S, Das SK, Jain A, Rout M, Dash R, Swain RK, Lee DY, Rusten TE, Chauhan S, Chauhan S. Cancer Res 81 315-331 (2021)
  7. Roquin2 suppresses breast cancer progression by inhibiting tumor angiogenesis via selectively destabilizing proangiogenic factors mRNA. Zhou M, Lu W, Li B, Yuan X, Liu M, Han J, Liu X, Li A. Int J Biol Sci 17 2884-2898 (2021)
  8. Structural basis for the recognition of transiently structured AU-rich elements by Roquin. Binas O, Tants JN, Peter SA, Janowski R, Davydova E, Braun J, Niessing D, Schwalbe H, Weigand JE, Schlundt A. Nucleic Acids Res 48 7385-7403 (2020)
  9. NMR-derived secondary structure of the full-length Ox40 mRNA 3'UTR and its multivalent binding to the immunoregulatory RBP Roquin. Tants JN, Becker LM, McNicoll F, Müller-McNicoll M, Schlundt A. Nucleic Acids Res 50 4083-4099 (2022)
  10. Construction of ceRNA regulatory networks for osteoporosis. Chen H, Wang H, Liu X, Li L, Abudusimu Y, Tuoheti Y. Mol Med Rep 28 145 (2023)


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