Cul4B regulates neural progenitor cell growth

BMC Neurosci. 2012 Sep 19:13:112. doi: 10.1186/1471-2202-13-112.

Abstract

Background: Cullin ubiquitin ligases are activated via the covalent modification of Cullins by the small ubiquitin-like protein nedd8 in a process called neddylation. Genetic mutations of cullin-4b (cul4b) cause a prevalent type of X-linked intellectual disability (XLID) in males, but the physiological function of Cul4B in neuronal cells remains unclear.

Results: There are three major isoforms of Cul4B (1, 2, and 3) in human and rodent tissues. By examining the endogenous Cul4B isoforms in the brain, this study demonstrates that Cul4B-1 and Cul4B-2 isoforms are unneddylated and more abundant in the brain whereas the lesser species Cul4B-3 that misses the N-terminus present in the other two isoforms is neddylated. The data suggest that the N-terminus of Cul4B inhibits neddylation in the larger isoforms. Immunostaining of human NT-2 cells also shows that most Cul4B is unneddylated, especially when it is localized in the process in G0-synchronized cells. This study demonstrates that Cul4B accumulates during mitosis and downregulation of Cul4B arrests NPCs and NT-2 cells in the G2/M phase of the cell cycle. In both human and rodent brain tissues, Cul4B-positive cells accumulate β-catenin in the dentate subgranular zone and the subventricular zone. These Cul4B-positive cells also co-express the MPM-2 mitotic epitope, suggesting that Cul4B is also necessary for mitosis progression in vivo.

Conclusions: This study provides first evidence that unneddylated Cul4B isoforms exist in the brain and are necessary for mitosis progression in NPCs. The data suggest that unneddylated Cul4B isoforms specifically inhibits β-catenin degradation during mitosis. Furthermore, unneddylated Cul4B may play a role in addition to cell cycle since it is exclusively localized to the processes in starved NT-2 cells. Further analyses of the different isoforms of Cul4B will help understand the cognitive deficits in Cul4B-linked XLID and give insights into drug and biomarker discoveries.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Bromodeoxyuridine / metabolism
  • Cell Cycle / physiology
  • Cell Growth Processes / physiology*
  • Cells, Cultured
  • Cerebral Cortex / cytology
  • Cerebral Ventricles / cytology
  • Cullin Proteins / genetics
  • Cullin Proteins / metabolism*
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Embryo, Mammalian
  • Female
  • Flow Cytometry
  • Forkhead Box Protein M1
  • Forkhead Transcription Factors / metabolism
  • Green Fluorescent Proteins / genetics
  • Hippocampus / metabolism
  • Humans
  • Immunoprecipitation
  • In Situ Nick-End Labeling
  • Intermediate Filament Proteins / genetics
  • Intermediate Filament Proteins / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mitosis / physiology
  • NEDD8 Protein
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Nestin
  • Neural Stem Cells / physiology*
  • Pregnancy
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • RNA, Small Interfering / pharmacology
  • Rats
  • Transfection
  • Ubiquitins / metabolism
  • beta Catenin / metabolism

Substances

  • CUL4B protein, human
  • Cullin Proteins
  • FOXM1 protein, human
  • Forkhead Box Protein M1
  • Forkhead Transcription Factors
  • Intermediate Filament Proteins
  • NEDD8 Protein
  • NEDD8 protein, human
  • NES protein, human
  • Nerve Tissue Proteins
  • Nes protein, mouse
  • Nes protein, rat
  • Nestin
  • Protein Isoforms
  • RNA, Small Interfering
  • Ubiquitins
  • beta Catenin
  • Green Fluorescent Proteins
  • Bromodeoxyuridine