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J. Biol. Chem., Vol. 279, Issue 20, 20672-20677, May 14, 2004

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Mitochondrial Respiratory Deficiencies Signal Up-regulation of Genes for Heat Shock Proteins^*

Evgeny V. Kuzmin¶, Olga V. Karpova, Thomas E. Elthon||, and Kathleen J. Newton**

From the Department of Biological Sciences, University of Missouri, Columbia, Missouri 65211 and the ^||School of Biological Sciences, University of Nebraska, Lincoln, Nebraska 68588

The consequences of mitochondrial dysfunction are not limited to the development of oxidative stress or initiation of apoptosis but can result in the establishment of stress tolerance. Using maize mitochondrial mutants, we show that permanent mitochondrial deficiencies trigger novel Ca²⁺-independent signaling pathways, leading to constitutive expression of genes for molecular chaperones, heat shock proteins (HSPs) of different classes. The signaling to activate hsp genes appears to originate from a reduced mitochondrial transmembrane potential. Upon depolarization of mitochondrial membranes in transient assays, gene induction for mitochondrial HSPs occurred more rapidly than that for cytosolic HSPs. We also demonstrate that in the nematode Caenorhabditis elegans transcription of hsp genes can be induced by RNA interference of nuclear respiratory genes. In both organisms, activation of hsp genes in response to mitochondrial impairment is distinct from their responses to heat shock and is not associated with oxidative stress. Thus, mitochondria-to-nucleus signaling to express a hsp gene network is apparently a widespread retrograde mechanism to facilitate cell defense and survival.

Received for publication, January 20, 2004 , and in revised form, February 20, 2004.

^* This work was supported by grants from the National Science Foundation and the Illinois-Missouri Biotechnology Alliance (to K. J. N. and T. E. E.). 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 two supplemental tables.

Both authors contributed equally to this work.

^¶ To whom correspondence may be addressed: Dept. of Biological Sciences, 324 Tucker Hall, University of Missouri, Columbia, MO 65211. Tel.: 573-882-40-49; Fax: 573-882-0123; E-mail: newtonk{at}missouri.edu. **To whom correspondence may be addressed: Dept. of Biological Sciences, 324 Tucker Hall, University of Missouri, Columbia, MO 65211. Tel.: 573-882-80-33; Fax: 573-882-0123; E-mail: bioscek{at}mchsi.com.

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