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J. Biol. Chem., Vol. 279, Issue 48, 49680-49688, November 26, 2004

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Phylogenetically Conserved Binding of Specific K Homology Domain Proteins to the 3'-Untranslated Region of the Vertebrate Middle Neurofilament mRNA^*

Amar Thyagarajan and Ben G. Szaro

From the Department of Biological Sciences and the Center for Neuroscience Research, University at Albany, State University of New York, Albany, New York 12222

As axons mature, neurofilament-M (NF-M) expression rises, contributing to maturation of the axonal cytoskeleton and an expansion in axon caliber. This increase is partly due to a rise in NF-M mRNA stability. Such post-transcriptional regulation is often mediated through the binding of specific proteins to the 3'-untranslated region (3'-UTR) of mRNAs. Vertebrate NF-M 3'-UTRs are remarkably well conserved, prompting us to test whether similar proteins bind the 3'-UTRs of different vertebrate NF-Ms. Identification of such proteins could lead to insights into the regulation of NF-M expression during development and in response to trauma or disease. Ultraviolet cross-linking analysis of proteins isolated from adult frog (Xenopus laevis), mouse, and rat brains revealed three ribonucleoprotein complexes (97, 70, and 47 kDa) that were present in all species and bound specifically to NF-M 3'-UTRs. Affinity purification of NF-M 3'-UTR-binding proteins from rat brain followed by mass spectrometry and immunoprecipitation assays identified heterogeneous nuclear ribonucleoprotein (hnRNP) K and hnRNP E1 as the proteins forming the 70- and 47-kDa complexes, respectively. These RNA-binding proteins of the KH domain family recognize CU-rich motifs identical to ones present in NF-M 3'-UTRs. Ultraviolet cross-linking assays performed on Xenopus embryos at different stages of neural development demonstrated that whereas hnRNP K binding occurred at all stages, hnRNP E binding occurred only at the most mature stages of axon development. Since hnRNP E is known to stabilize mRNAs, these results raise the hypothesis that these proteins may contribute to the increases in cytoplasmic levels of NF-M mRNA that accompany axonal maturation.

Received for publication, August 4, 2004

^* This work was supported by the National Science Foundation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Dept. of Biological Sciences, University at Albany, SUNY, 1400 Washington Ave., Albany, NY 12222. Tel.: 518-442-4364; Fax: 518-442-4767; E-mail: bgs86{at}cnsunix.albany.edu.

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