Expression of Leukemia-Associated Nup98 Fusion Proteins Generates an Aberrant Nuclear Envelope Phenotype

PLoS One. 2016 Mar 31;11(3):e0152321. doi: 10.1371/journal.pone.0152321. eCollection 2016.

Abstract

Chromosomal translocations involving the nucleoporin NUP98 have been described in several hematopoietic malignancies, in particular acute myeloid leukemia (AML). In the resulting chimeric proteins, Nup98's N-terminal region is fused to the C-terminal region of about 30 different partners, including homeodomain (HD) transcription factors. While transcriptional targets of distinct Nup98 chimeras related to immortalization are relatively well described, little is known about other potential cellular effects of these fusion proteins. By comparing the sub-nuclear localization of a large number of Nup98 fusions with HD and non-HD partners throughout the cell cycle we found that while all Nup98 chimeras were nuclear during interphase, only Nup98-HD fusion proteins exhibited a characteristic speckled appearance. During mitosis, only Nup98-HD fusions were concentrated on chromosomes. Despite the difference in localization, all tested Nup98 chimera provoked morphological alterations in the nuclear envelope (NE), in particular affecting the nuclear lamina and the lamina-associated polypeptide 2α (LAP2α). Importantly, such aberrations were not only observed in transiently transfected HeLa cells but also in mouse bone marrow cells immortalized by Nup98 fusions and in cells derived from leukemia patients harboring Nup98 fusions. Our findings unravel Nup98 fusion-associated NE alterations that may contribute to leukemogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Cells / metabolism
  • Bone Marrow Cells / pathology
  • Cell Cycle
  • DNA-Binding Proteins / analysis
  • DNA-Binding Proteins / metabolism
  • HeLa Cells
  • Homeodomain Proteins / analysis
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Leukemia, Myeloid, Acute / genetics
  • Leukemia, Myeloid, Acute / metabolism
  • Leukemia, Myeloid, Acute / pathology
  • Membrane Proteins / analysis
  • Membrane Proteins / metabolism
  • Mice
  • Mitosis
  • Nuclear Envelope / genetics*
  • Nuclear Envelope / metabolism
  • Nuclear Envelope / pathology*
  • Nuclear Pore Complex Proteins / analysis
  • Nuclear Pore Complex Proteins / genetics*
  • Nuclear Pore Complex Proteins / metabolism
  • Oncogene Proteins, Fusion / analysis
  • Oncogene Proteins, Fusion / genetics*
  • Oncogene Proteins, Fusion / metabolism
  • Phenotype
  • Translocation, Genetic

Substances

  • DNA-Binding Proteins
  • Homeodomain Proteins
  • Membrane Proteins
  • Nuclear Pore Complex Proteins
  • Oncogene Proteins, Fusion
  • lamina-associated polypeptide 2
  • nuclear pore complex protein 98

Grants and funding

This work was supported by Fonds de la Recherche Scientifique-FNRS: grant numbers T.0237.13 and 7.4595.14; (www.frs-fnrs.be); the Swiss National Science Foundation: grant number 31003A_149714, (www.sf.ch); and the Swiss Cancer League, grant number: KFS-3019-08-2012, (www.krebsliga.ch).