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J. Biol. Chem., Vol. 279, Issue 25, 25959-25965, June 18, 2004

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Ruthenium Red-induced Bundling of Bacterial Cell Division Protein, FtsZ^*

Manas Kumar Santra, Tushar K. Beuria, Abhijit Banerjee, and Dulal Panda

From the School of Biosciences and Bioengineering, Indian Institute of Technology, Bombay, Powai, Mumbai 400076, India

The assembly of FtsZ plays a major role in bacterial cell division, and it is thought that the assembly dynamics of FtsZ is a finely regulated process. Here, we show that ruthenium red is able to modulate FtsZ assembly in vitro. In contrast to the inhibitory effects of ruthenium red on microtubule polymerization, we found that a substoichiometric concentration of ruthenium red strongly increased the light-scattering signal of FtsZ assembly. Further, sedimentable polymer mass was increased by 1.5- and 2-fold in the presence of 2 and 10 µM ruthenium red, respectively. In addition, ruthenium red strongly reduced the GTPase activity and prevented dilution-induced disassembly of FtsZ polymers. Electron microscopic analysis showed that 4–10 µM of ruthenium red produced thick bundles of FtsZ polymers. The significant increase in the light-scattering signal and pelletable polymer mass in the presence of ruthenium red seemed to be due to the bundling of FtsZ protofilaments into larger polymers rather than the actual increase in the level of polymeric FtsZ. Furthermore, ruthenium red was found to copolymerize with FtsZ, and the copolymerization of substoichiometric amounts of ruthenium red with FtsZ polymers promoted cooperative assembly of FtsZ that produced large bundles. Calcium inhibited the binding of ruthenium red to FtsZ. However, a concentration of calcium 1000-fold higher than that of ruthenium red was required to produce similar effects on FtsZ assembly. Ruthenium red strongly modulated FtsZ polymerization, suggesting the presence of an important regulatory site on FtsZ and suggesting that a natural ligand, which mimics the action of ruthenium red, may regulate the assembly of FtsZ in bacteria.

Received for publication, November 14, 2003 , and in revised form, March 15, 2004.

^* This study was funded by a grant from the Department of Science and Technology, Government of India (to D. P.). 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.

Supported by a fellowship from the Council of Scientific and Industrial Research, Government of India.

To whom correspondence should be addressed. Tel.: 91-22-2576-7838; Fax: 91-22-2572-3480; E-mail: panda{at}iitb.ac.in.

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