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J. Biol. Chem., Vol. 280, Issue 20, 19461-19471, May 20, 2005

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Human Tumorous Imaginal Disc 1 (TID1) Associates with Trk Receptor Tyrosine Kinases and Regulates Neurite Outgrowth in nnr5-TrkA Cells^*

Hui-Yu Liu, James I. S. MacDonald, Todd Hryciw, Chunhui Li, and Susan O. Meakin¶||**

From the Cell Biology Group, Robarts Research Institute, London, Ontario N6A 5K8 and the ^¶Department of Biochemistry and ^||The Graduate Program in Neuroscience, University of Western Ontario, London, Ontario N6A 5C1, Canada

The human tumorous imaginal disc 1 (TID1) proteins including TID1_L and TID1_S, members of the DnaJ domain protein family, are involved in multiple intracellular signaling pathways such as apoptosis induction, cell proliferation, and survival. Here we report that TID1 associates with the Trk receptor tyrosine kinases and regulates nerve growth factor (NGF)-induced neurite outgrowth in PC12-derived nnr5 cells. Binding assays and transfection studies showed that the carboxyl-terminal end of TID1 (residues 224–429) bound to Trk at the activation loop (Tyr(P)⁶⁸³-Tyr⁶⁸⁴(P)⁶⁸⁴ in rat TrkA) and that TID1 was tyrosine phosphorylated by Trk both in yeast and in transfected cells. Moreover endogenous TID1 was also tyrosine phosphorylated by and co-immunoprecipitated with Trk in neurotrophin-stimulated primary rat hippocampal neurons. Overexpression studies showed that both TID1_L and TID1_S significantly facilitated NGF-induced neurite outgrowth in TrkA-expressing nnr5 cells possibly through a mechanism involving increased activation of mitogen-activated protein kinase. Consistently knockdown of endogenous TID1, mediated with specific short hairpin RNA, significantly reduced NGF-induced neurite growth in nnr5-TrkA cells. These data provide the first evidence that TID1 is a novel intracellular adaptor that interacts with the Trk receptor tyrosine kinases in an activity-dependent manner to facilitate Trk-dependent intracellular signaling.

Received for publication, January 10, 2005 , and in revised form, February 25, 2005.

^* This work was supported by an operating grant from The Cancer Research Society Inc. and by an EJLB Foundation scholar research program grant (to S. O. M.). 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.

A Canadian Institutes of Health Research fellow.

^** To whom correspondence should be addressed: Cell Biology Group, Robarts Research Inst., London, Ontario N6A 5K8, Canada. Tel.: 519-663-5777 (ext. 34304); Fax: 519-663-3789; E-mail: smeakin{at}robarts.ca.

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