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J. Biol. Chem., Vol. 279, Issue 37, 38820-38829, September 10, 2004

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Nucleocytoplasmic Shuttling of Receptor-interacting Protein 3 (RIP3)

IDENTIFICATION OF NOVEL NUCLEAR EXPORT AND IMPORT SIGNALS IN RIP3^*

Yonghui Yang, Jun Ma, Youjun Chen, and Mian Wu¶

From the Hefei National Laboratory for Physical Sciences at Microscale and School of Life Sciences, University of Science and Technology of China, Hefei, Anhui 230026, People's Republic of China and the School of Biological Sciences, Nanyang Technological University, 60 Nanyang Dr., Singapore 637551

Receptor-interacting protein 3 (RIP3), a member of the RIP Ser/Thr kinase family, has been characterized as a pro-apoptotic protein involved in the tumor necrosis factor receptor-1 signaling pathway. In this study, we have mapped a minimal region of RIP3 sufficient for apoptosis induction to a fragment of 31 amino acids in length. This minimal region also functions as an unconventional nuclear localization signal sufficient to confer the import of full-length RIP3 to the nucleus to trigger apoptosis, suggesting that RIP3 is able to play an apoptosis-inducing role in the nucleus. In addition, we have characterized two novel leucine-rich nuclear export signals (NESs) that are responsible for the nuclear export of RIP3 to the cytoplasm via a chromosome region maintenance 1 (CRM1)-dependent pathway and an extra leucine-rich NES in the N terminus of RIP3 that contributes to the cytoplasmic distribution in a CRM1-independent manner. Thus, we provide the first evidence that RIP3 acts a nucleocytoplasmic shuttling protein, which presents a possible link between death receptor signaling and nuclear apoptosis.

Received for publication, February 15, 2004 , and in revised form, June 17, 2004.

^* This work was supported by the Key Project Fund (KSCX2-2-01-004) from the Chinese Academy of Sciences, by the National Natural Science Foundation of China (Grants 90208027, 30370308, and 30121001), and by a 973 Grant (2002CB713702) from the Ministry of Science and Technology of China. 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. Tel.: 86-551-360-7324; Fax: 86-551-360-6264; E-mail: wumian88{at}yahoo.com.

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