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J. Biol. Chem., Vol. 278, Issue 48, 47915-47921, November 28, 2003

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Temperature-controlled Structural Alterations of an RNA Thermometer^*

Saheli Chowdhury, Curdin Ragaz, Emma Kreuger, and Franz Narberhaus

From the Institut of Microbiology, Eidgenössische Technische Hochschule, Schmelzbergstrasse 7, CH-8092 Zürich, Switzerland

Thermoresponsive structures in the 5'-untranslated region of mRNA are known to control translation of heat shock and virulence genes. Expression of many rhizobial heat shock genes is regulated by a conserved sequence element called ROSE for repression of heat shock gene expression. This cis-acting, untranslated mRNA is thought to prevent ribosome access at low temperature through an extended secondary structure, which partially melts when the temperature rises. We show here by a series of in vivo and in vitro approaches that ROSE is a sensitive thermometer responding in the physiologically relevant temperature range between 30 and 40 °C. Point mutations predicted to disrupt base pairing enhanced expression at 30 °C. Compensatory mutations restored repression, emphasizing the importance of secondary structures in the sensory RNA. Only moderate inducibility of a 5'-truncated ROSE variant suggests that interactions between individual stem loops coordinate temperature sensing. In the presence of a complementary oligonucleotide, the functionally important stem loop of ROSE was rendered susceptible to RNase H treatment at heat shock temperatures. Since major structural rearrangements were not observed during UV and CD spectroscopy, subtle structural changes involving the Shine-Dalgarno sequence are proposed to mediate translational control. Temperature perception by the sensory RNA is an ordered process that most likely occurs without the aid of accessory factors.

Received for publication, June 27, 2003 , and in revised form, September 5, 2003.

^* This work was supported in part by the Swiss Federal Institute of Technology, Zürich. 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 student at Stockholm University, Sweden. Supported by an ERASMUS scholarship.

To whom correspondence should be addressed. Tel.: 41-1-632-2586; Fax: 41-1-632-1148; E-mail: fnarber{at}micro.biol.ethz.ch.

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