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J. Biol. Chem., Vol. 279, Issue 17, 17434-17442, April 23, 2004

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Conserved Nuclear Export Sequences in Schizosaccharomyces pombe Mex67 and Human TAP Function in mRNA Export by Direct Nuclear Pore Interactions^*

Anjan G. Thakurta, Ganesh Gopal, Jin Ho Yoon¶, Tapas Saha||, and Ravi Dhar**

From the Center for Cancer Research, NCI and ^||NICHD, National Institutes of Health, Bethesda, Maryland 20892, the Department of Biology, Sungshin Women's University, Dongseon-dong 3 ka 249-1, Seongbuk-gu, Seoul 136-742, South Korea, and the ^¶Division of Biology, College of Natural Sciences, Kangnung National University, Gangneung 210-702, South Korea

Mex67, the homolog of human TAP, is not an essential mRNA export factor in Schizosaccharomyces pombe. Here we show that S. pombe encodes a homolog of the TAP cofactor that we have also named p15, whose function in mRNA export is not essential. We have identified and characterized two distinct nuclear export activities, nuclear export signal (NES) I and NES II, within the region of amino acids 434–509 of Mex67. These residues map within the known NTF2-like fold of TAP (amino acids 371–551). We show that the homologs of these two NESs are present and are functionally conserved in TAP. The NES I, NES II, and NES I + II of TAP and Mex67 directly bind with -phenylalanine-glycine (-FG)-containing sequences of S. pombe Nup159 and Nup98 but not with human p62. Mutants of NES I or NES II of Mex67/TAP that do not bind -FG Nup159 and Nup98 in vitro are unable to mediate nuclear export of a heterologous protein in S. pombe and in HeLa cells. Fused with the RNA recognition motifs (RRMs) of Crp79 and green fluorescent protein (GFP) (RRM-NES-GFP), the NES I and NES II of Mex67 or TAP can suppress the mRNA export defect of the p15 rae1-167 synthetic lethal S. pombe strain, suggesting that the NESs can function in the absence of p15. These novel nuclear export sequences may provide additional routes for delivering Mex67/TAP to the nuclear pore complex.

Received for publication, September 2, 2003 , and in revised form, February 4, 2004.

^* 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: NCI, National Institutes of Health, Bldg. 37/Rm. 6138, 9000 Rockville Pike, Bethesda, MD 20892-4260. Tel.: 301-496-0990; Fax: 301-480-5088; E-mail: dharr{at}mail.nih.gov.

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