Depletion of guanine nucleotides leads to the Mdm2-dependent proteasomal degradation of nucleostemin

Cancer Res. 2009 Apr 1;69(7):3004-12. doi: 10.1158/0008-5472.CAN-08-3413. Epub 2009 Mar 24.

Abstract

Nucleostemin is a positive regulator of cell proliferation and is highly expressed in a variety of stem cells, tumors, and tumor cell lines. The protein shuttles between the nucleolus and the nucleus in a GTP-dependent fashion. Selective depletion of intracellular guanine nucleotides by AVN-944, an inhibitor of the de novo purine synthetic enzyme, IMP dehydrogenase, leads to the rapid disappearance of nucleostemin protein in tumor cell lines, an effect that does not occur with two other nucleolar proteins, nucleophosmin or nucleolin. Endogenous nucleostemin protein is completely stabilized by MG132, an inhibitor of the 26S proteasome, as are the levels of expressed enhanced green fluorescent protein-tagged nucleostemin, both wild-type protein and protein containing mutations at the G(1) GTP binding site. Nutlin-3a, a small molecule that disrupts the binding of the E3 ubiquitin ligase, Mdm2, to p53, stabilizes nucleostemin protein in the face of guanine nucleotide depletion, as does siRNA-mediated knockdown of Mdm2 expression and overexpression of a dominant-negative form of Mdm2. Neither Doxorubicin nor Actinomycin D, which cause the release of nucleostemin from the nucleolus, results in nucleostemin degradation. We conclude that nucleostemin is a target for Mdm2-mediated ubiquitination and degradation when not bound to GTP. Because this effect does not occur with other chemotherapeutic agents, the induction of nucleostemin protein degradation in tumor cells by IMP dehydrogenase inhibition or by other small molecules that disrupt GTP binding may offer a new approach to the treatment of certain neoplastic diseases.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carbamates / pharmacology
  • Carrier Proteins / biosynthesis
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Line, Tumor
  • GTP-Binding Proteins
  • Guanosine Triphosphate / deficiency
  • Guanosine Triphosphate / metabolism*
  • Humans
  • IMP Dehydrogenase / antagonists & inhibitors
  • Imidazoles / pharmacology
  • K562 Cells
  • Nuclear Proteins / biosynthesis
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Nucleolin
  • Phenylurea Compounds / pharmacology
  • Phosphoproteins / metabolism
  • Piperazines / pharmacology
  • Proteasome Endopeptidase Complex / metabolism*
  • Proteasome Inhibitors
  • Proto-Oncogene Proteins c-mdm2 / antagonists & inhibitors
  • Proto-Oncogene Proteins c-mdm2 / metabolism*
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • RNA-Binding Proteins / metabolism

Substances

  • Carbamates
  • Carrier Proteins
  • GNL3 protein, human
  • Imidazoles
  • Nuclear Proteins
  • Phenylurea Compounds
  • Phosphoproteins
  • Piperazines
  • Proteasome Inhibitors
  • RNA, Messenger
  • RNA-Binding Proteins
  • nutlin 3
  • Guanosine Triphosphate
  • IMP Dehydrogenase
  • MDM2 protein, human
  • Proto-Oncogene Proteins c-mdm2
  • Proteasome Endopeptidase Complex
  • GTP-Binding Proteins
  • AVN 944