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J. Biol. Chem., Vol. 281, Issue 15, 10461-10472, April 14, 2006

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Positioned Nucleosomes Due to Sequential Remodeling of the Yeast U6 Small Nuclear RNA Chromatin Are Essential for Its Transcriptional Activation^*

From the Centre for Cellular and Molecular Biology, Uppal Road, Tarnaka, Hyderabad 500007, India

Transcription from the yeast SNR6 (U6 small nuclear RNA) chromatin, a gene transcribed by the enzyme RNA polymerase III, depends on its transcription factor IIIC (TFIIIC) and the promoter elements (the intragenic box A and box B located downstream to its terminator) to which TFIIIC binds. The genes transcribed by polymerase III generally lack the upstream promoter elements where TFIIIC is known to recruit the transcription initiation factor TFIIIB. The TFIIIC-dependent chromatin remodeling of the gene in vitro that involves translational positioning of a nucleosome between boxes A and B is found to be essential for its transcriptional activation. We show here that the role of TFIIIC is not limited to the recruitment of TFIIIB on chromatin templates. The pre-binding of TFIIIB to the SNR6 TATA box in the upstream gene region does not alleviate TFIIIC requirement for transcriptional activation of the chromatin. Binding of TFIIIC to an array of pre-positioned nucleosomes results in an upward shift of the single nucleosome between boxes A and B. The 40-bp shift of this nucleosome in the 3' to 5' direction leads to increased nuclease sensitivity of the 40-bp DNA 3' to the upstream TATA box. Further chromatin remodeling accompanies the binding of TFIIIB in the next step. This two-step remodeling mechanism using the basal factors of the gene yields high transcription levels and generates a chromatin structure similar to that reported for the gene in vivo.

Received for publication, November 21, 2005 , and in revised form, December 30, 2005.

^* This work was supported in part by the Council of Scientific and Industrial Research, Government of India. 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 Recipient of Senior Research fellowship from the Council of Scientific and Industrial Research. Present address: Institute for Cellular and Molecular Biology, MBB 3.212, University of Texas at Austin, 2500 Speedway, Austin, TX 78712-0159.

² To whom correspondence should be addressed: Centre for Cellular and Molecular Biology, Uppal Rd., Tarnaka, Hyderabad-500007, India. Tel.: 91-40-27192603; Fax: 91-40-27160591; E-mail: purnima{at}ccmb.res.in.

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