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J. Biol. Chem., Vol. 282, Issue 5, 3042-3049, February 2, 2007

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Actively Transcribed GAL Genes Can Be Physically Linked to the Nuclear Pore by the SAGA Chromatin Modifying Complex^*

Roopa Luthra¹, Shana C. Kerr¹, Michelle T. Harreman², Luciano H. Apponi^¶, Milo B. Fasken, Suneela Ramineni^||, Shyam Chaurasia^||, Sandro R. Valentini^¶, and Anita H. Corbett³

From the Departments of Biochemistry and ^||Pharmacology and Graduate Program in Biochemistry, Cell, and Developmental Biology, Emory University School of Medicine, Atlanta, Georgia 30322 and the ^¶Department of Biological Sciences, School of Pharmaceutical Sciences, São Paulo State University, UNESP, Araraquara, San Paulo, 14801-902 Brazil

Recent work has demonstrated that some actively transcribed genes closely associate with nuclear pore complexes (NPC) at the nuclear periphery. The Saccharomyces cerevisiae Mlp1 and Mlp2 proteins are components of the inner nuclear basket of the nuclear pore that mediate interactions with these active genes. To investigate the physical link between the NPC and active loci, we identified proteins that interact with the carboxyl-terminal globular domain of Mlp1 by tandem affinity purification coupled with mass spectrometry. This analysis led to the identification of several components of the Spt-Ada-Gcn5-acetyltransferase (SAGA) histone acetyltransferase complex, Gcn5, Ada2, and Spt7. We utilized co-immunoprecipitation and in vitro binding assays to confirm the interaction between the Mlp proteins and SAGA components. Chromatin immunoprecipitation experiments revealed that Mlp1 and SAGA components associate with the same region of the GAL promoters. Critically, this Mlp-promoter interaction depends on the integrity of the SAGA complex. These results identify a physical association between SAGA and the NPC, and support previous results that relied upon visualization of GAL loci at the nuclear periphery by microscopy (Cabal, G. G. Genovesio, A., Rodriguez-Navarro, S., Zimmer, C., Gadal, O., Lesne, A., Buc, H., Feuerbach-Fournier, F., Olivo-Marin, J.-C., Hurt, E. C., and Nehrbass, U. (2006) Nature 441, 770–773). We propose that a physical interaction between nuclear pore components and the SAGA complex can link the actively transcribed GAL genes to the nuclear pore.

Received for publication, September 11, 2006 , and in revised form, December 4, 2006.

^* This work was supported by a grant from the National Institutes of Health (to A. H. C.) and a training grant from the National Institutes of Health (to S. C. K.). 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.

¹ Both authors contributed equally to this work.

² Present address: Cancer Research UK, Clare Hall Laboratories, Blanche Lane, South Mimms, Hertfordshire EN6 3LD, United Kingdom.

³ To whom correspondence should be addressed: 1510 Clifton Rd., NE, Atlanta, GA 30322. Tel.: 404-727-4546; Fax: 404-727-3954; E-mail: acorbe2{at}emory.edu.

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