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The Journal of Neuroscience, June 14, 2006, 26(24):6496-6508; doi:10.1523/JNEUROSCI.0649-06.2006

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Cellular/Molecular
Dendritic Localization of the Translational Repressor Pumilio 2 and Its Contribution to Dendritic Stress Granules

John P. Vessey,¹ Angelo Vaccani,^1,2 Yunli Xie,¹ Ralf Dahm,¹ Daniela Karra,¹ Michael A. Kiebler,¹ and Paolo Macchi¹

¹Division of Neural Cell Biology, Center for Brain Research, Medical University of Vienna, A-1090 Vienna, Austria, and ²Department of Structural and Functional Biology, Pharmacology Section, Center of Neurosciences, University of Insubria, 21052 Busto Arsizio (VA), Italy

Correspondence should be addressed to Paolo Macchi, Division of Neuronal Cell Biology, Center for Brain Research, Medical University of Vienna, Spitalgasse 4, A-1090 Vienna, Austria. Email: paolo.macchi{at}meduniwien.ac.at

Pumilio (Pum) protein acts as a translational inhibitor in several organisms including yeast, Drosophila, Xenopus, and mammals. Two Pumilio genes, Pum1 and Pum2, have been identified in mammals, but their function in neurons has not been identified. In this study, we found that Pum2 mRNA is expressed during neuronal development and that the protein is found in discrete particles in both the cell body and the dendritic compartment of fully polarized neurons. This finding indicates that Pum2 is a novel candidate of dendritically localized ribonucleoparticles (RNPs). During metabolic stress, Pum2 is present in stress granules (SGs), which are subsequently detected in the somatodendritic domain. It remains excluded from processing bodies under all conditions. When overexpressed in neurons and fibroblasts, Pum2 induces the formation of SGs that also contain T-cell intracellular antigen 1 (TIA-1)-related protein, eukaryotic initiation factor 4E, poly(A)-binding protein, TIA-1, and other RNA-binding proteins including Staufen1 and Barentsz. This induction of SGs is dependent on the RNA-binding domain and a glutamine-rich region in the N terminus of Pum2. This glutamine-rich region behaves in a similar manner as TIA-1 and prion protein, two molecules with known roles in protein aggregation. Pum2 downregulation in neurons via RNA interference (RNAi) interferes with the formation of SGs during metabolic stress. Cotransfection with an RNAi-resistant portion of the Pum2 mRNA restores SG formation. These results suggest a role for Pum2 in dendritic RNPs and SG formation in mammalian neurons.

Key words: Pumilio 2; dendrite; stress granule; hippocampal neurons; RNA-binding proteins; ribonucleoparticles

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Received Feb. 14, 2006; revised April 5, 2006; accepted May 3, 2006.

Correspondence should be addressed to Paolo Macchi, Division of Neuronal Cell Biology, Center for Brain Research, Medical University of Vienna, Spitalgasse 4, A-1090 Vienna, Austria. Email: paolo.macchi{at}meduniwien.ac.at

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