Involvement in surface antigen expression by a moonlighting FG-repeat nucleoporin in trypanosomes

Jennifer M. Holden, Ludek Koreny, Samson Obado, Alexander V. Ratushny, Wei-Ming Chen, Jean-Mathieu Bart, Miguel Navarro, Brian T. Chait, John D. Aitchison, Michael P. Rout, Mark C. Field (Lead / Corresponding author)

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Abstract

Components of the nuclear periphery coordinate a multitude of activities, including macromolecular transport, cell-cycle progression and chromatin organization. Nuclear pore complexes (NPCs) mediate nucleocytoplasmic transport, mRNA processing and transcriptional regulation, and NPC components can define regions of high transcriptional activity in some organisms at the nuclear periphery and nucleoplasm. Lineage-specific features underpin several core nuclear functions, and in trypanosomatids, which branched very early from other eukaryotes, unique protein components constitute the lamina, kinetochores and parts of the NPCs. Here we describe an FG-repeat nucleoporin, TbNup53b, that has dual localizations within the nucleoplasm and NPC. In addition to association with nucleoporins, TbNup53b interacts with a knowntrans-splicing component, TSR1, and has a role in controlling expression of surface proteins including the nucleolar periphery-located, procyclin genes. Significantly, while several nucleoporins are implicated in intranuclear transcriptional regulation in metazoa, TbNup53b appears orthologous to components of the yeast/human Nup49/Nup58 complex, for which no transcriptional functions are known. These data suggest that FG-Nups are frequently co-opted to transcriptional functions during evolution, and extends the presence of FG-repeat nucleoporin control of gene expression to trypanosomes, suggesting this is a widespread and ancient eukaryotic feature, as well as underscoring once more flexibility within nucleoporin function.

Original languageEnglish
Pages (from-to)1100-1110
Number of pages11
JournalMolecular Biology of the Cell
Volume29
Issue number9
Early online date3 Mar 2018
DOIs
Publication statusPublished - 1 May 2018

Keywords

  • Journal article
  • Trypanosoma brucei
  • Nuclear pore complex
  • Procyclin
  • Gene expression
  • Splicing
  • mRNA quality

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    Holden, J. M., Koreny, L., Obado, S., Ratushny, A. V., Chen, W-M., Bart, J-M., Navarro, M., Chait, B. T., Aitchison, J. D., Rout, M. P., & Field, M. C. (2018). Involvement in surface antigen expression by a moonlighting FG-repeat nucleoporin in trypanosomes. Molecular Biology of the Cell, 29(9), 1100-1110. https://doi.org/10.1091/mbc.E17-06-0430