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J. Biol. Chem., Vol. 280, Issue 36, 31981-31990, September 9, 2005

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Nuclear Export Factor Family Protein Participates in Cytoplasmic mRNA Trafficking^*

Irina Tretyakova, Andrei S. Zolotukhin, Wei Tan, Jenifer Bear, Friedrich Propst¶, Gordon Ruthel||, and Barbara K. Felber**

From the Human Retrovirus Pathogenesis Section, Vaccine Branch, Center for Cancer Research, NCI-Frederick, National Institutes of Health, Frederick, Maryland 21702, ^¶Institute of Biochemistry and Molecular Cell Biology, University of Vienna, Vienna Biocenter, Dr. Bohr-Gasse 9, A-1030 Vienna, Austria, and ^||Goldbelt Raven, LLC, Fort Detrick, Maryland 21702

In eukaryotes, the nuclear export of mRNA is mediated by nuclear export factor 1 (NXF1) receptors. Metazoans encode additional NXF1-related proteins of unknown function, which share homology and domain organization with NXF1. Some mammalian NXF1-related genes are expressed preferentially in the brain and are thought to participate in neuronal mRNA metabolism. To address the roles of NXF1-related factors, we studied the two mouse NXF1 homologues, mNXF2 and mNXF7. In neuronal cells, mNXF2, but not mNXF7, exhibited mRNA export activity similar to that of Tip-associated protein/NXF1. Surprisingly, mNXF7 incorporated into mobile particles in the neurites that contained poly(A) and ribosomal RNA and colocalized with Staufen1-containing transport granules, indicating a role in neuronal mRNA trafficking. Yeast two-hybrid interaction, coimmunoprecipitation, and in vitro binding studies showed that NXF proteins bound to brain-specific microtubule-associated proteins (MAP) such as MAP1B and the WD repeat protein Unrip. Both in vitro and in vivo, MAP1B also bound to NXF export cofactor U2AF as well as to Staufen1 and Unrip. These findings revealed a network of interactions likely coupling the export and cytoplasmic trafficking of mRNA. We propose a model in which MAP1B tethers the NXF-associated mRNA to microtubules and facilitates their translocation along dendrites while Unrip provides a scaffold for the assembly of these transport intermediates.

Received for publication, March 11, 2005 , and in revised form, July 12, 2005.

^* 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.

Both authors contributed equally to this work.

^** To whom correspondence should be addressed: Human Retrovirus Pathogenesis Section, NCI-Frederick, National Institutes of Health, Bldg. 535, Rm. 209, Frederick, MD 21702-1201. Tel.: 301-846-5159; Fax: 301-846-7146; E-mail: felber{at}mail.ncifcrf.gov.

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