A novel mutation in the upstream open reading frame of the CDKN1B gene causes a MEN4 phenotype

PLoS Genet. 2013 Mar;9(3):e1003350. doi: 10.1371/journal.pgen.1003350. Epub 2013 Mar 21.

Abstract

The CDKN1B gene encodes the cyclin-dependent kinase inhibitor p27(KIP1), an atypical tumor suppressor playing a key role in cell cycle regulation, cell proliferation, and differentiation. Impaired p27(KIP1) expression and/or localization are often observed in tumor cells, further confirming its central role in regulating the cell cycle. Recently, germline mutations in CDKN1B have been associated with the inherited multiple endocrine neoplasia syndrome type 4, an autosomal dominant syndrome characterized by varying combinations of tumors affecting at least two endocrine organs. In this study we identified a 4-bp deletion in a highly conserved regulatory upstream ORF (uORF) in the 5'UTR of the CDKN1B gene in a patient with a pituitary adenoma and a well-differentiated pancreatic neoplasm. This deletion causes the shift of the uORF termination codon with the consequent lengthening of the uORF-encoded peptide and the drastic shortening of the intercistronic space. Our data on the immunohistochemical analysis of the patient's pancreatic lesion, functional studies based on dual-luciferase assays, site-directed mutagenesis, and on polysome profiling show a negative influence of this deletion on the translation reinitiation at the CDKN1B starting site, with a consequent reduction in p27(KIP1) expression. Our findings demonstrate that, in addition to the previously described mechanisms leading to reduced p27(KIP1) activity, such as degradation via the ubiquitin/proteasome pathway or non-covalent sequestration, p27(KIP1) activity can also be modulated by an uORF and mutations affecting uORF could change p27(KIP1) expression. This study adds the CDKN1B gene to the short list of genes for which mutations that either create, delete, or severely modify their regulatory uORFs have been associated with human diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5' Untranslated Regions
  • Cell Cycle
  • Cell Differentiation
  • Cell Proliferation
  • Cyclin-Dependent Kinase Inhibitor p27* / genetics
  • Cyclin-Dependent Kinase Inhibitor p27* / metabolism
  • Genetic Predisposition to Disease*
  • HeLa Cells
  • Humans
  • Multiple Endocrine Neoplasia / genetics*
  • Multiple Endocrine Neoplasia / metabolism
  • Multiple Endocrine Neoplasia / pathology
  • Mutagenesis, Site-Directed
  • Mutation
  • Open Reading Frames / genetics
  • Protein Biosynthesis*

Substances

  • 5' Untranslated Regions
  • CDKN1B protein, human
  • Cyclin-Dependent Kinase Inhibitor p27

Supplementary concepts

  • Multiple Endocrine Neoplasia, Type IV

Grants and funding

This work was supported by the Italian Ministry of University and Research (grant 2009YJTBAZ_003) and by the University of Padova (grant CPDA105053/10). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.