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J. Biol. Chem., Vol. 279, Issue 44, 46008-46013, October 29, 2004

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A Unifying Model for the Role of Polyamines in Bacterial Cell Growth, the Polyamine Modulon^*

Madoka Yoshida, Keiko Kashiwagi, Ai Shigemasa, Shiho Taniguchi, Kaneyoshi Yamamoto, Hideki Makinoshima¶, Akira Ishihama¶, and Kazuei Igarashi||

From the Graduate School of Pharmaceutical Sciences, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8675, Japan, the Graduate School of Agriculture of Kinki University, 3327-204, Nakamachi, Nara 631-8505, Japan, and the ^¶Division of Molecular Biology, Nippon Institute for Biological Science, Ome, Tokyo 198-0024, Japan

We reported previously that the synthesis of specific proteins such as OppA, Cya, and RpoS (³⁸), which are important for cell growth and viability, is stimulated by polyamines at the level of translation. In this study we found that the synthesis of FecI and Fis was also stimulated by polyamines at the level of translation. The FecI and Fis proteins enhance the expression of mRNAs that are involved in iron uptake and energy metabolism and the expression of rRNA and some tRNAs. The Shine-Dalgarno (SD) sequence of their mRNAs was not obvious or was not located at the usual position. When the SD sequences were created at the normal position on these mRNAs, protein synthesis was no longer influenced by polyamines. Thus, the common characteristic of these mRNAs was to have a weak or ineffective SD sequence. We propose that a group of genes whose expression is enhanced by polyamines at the level of translation be referred to as a "polyamine modulon." By DNA microarray, we found that 309 of 2,742 mRNA species were upregulated by polyamines. Among the 309 up-regulated genes, transcriptional enhancement of at least 58 genes might be attributable to increased levels of the transcription factors Cya, RpoS, FecI, and Fis, which are all organized in the polyamine modulon. This unifying molecular mechanism is proposed to underlie the physiological role of polyamines in controlling the growth of Escherichia coli.

Received for publication, April 21, 2004 , and in revised form, July 30, 2004.

^* This work was supported by a grant-in-aid for Scientific Research on Priority Areas (A) "Genome Biology" from the Ministry of Education, Culture, Sports, Science and Technology of Japan. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental data in the form of tables containing detailed information on genes up- or down-regulated in the presence of putrescine.

^|| To whom correspondence should be addressed. Tel.: 81-43-226-2871; Fax: 81-43-226-2873; E-mail: iga16077{at}p.chiba-u.ac.jp.

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