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Originally published In Press as doi:10.1074/jbc.M003024200 on August 4, 2000

J. Biol. Chem., Vol. 275, Issue 42, 33123-33133, October 20, 2000
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Differential Regulation of the Catalytic and Accessory Subunit Genes of Drosophila Mitochondrial DNA Polymerase*

Etienne LefaiDagger §, Miguel A. Fernández-MorenoDagger §, Anuradha Alahari||, Laurie S. Kaguni||, and Rafael GaresseDagger **

From the Dagger  Departamento de Bioquímica, Instituto de Investigaciones Biomédicas "Alberto Sols" CSIC-UAM, Facultad de Medicina, Universidad Autónoma de Madrid, c/Arzobispo Morcillo 4, 28029 Madrid, Spain and the || Department of Biochemistry, Michigan State University, East Lansing, Michigan 48824-1319

The developmental pattern of expression of the genes encoding the catalytic (alpha ) and accessory (beta ) subunits of mitochondrial DNA polymerase (pol gamma ) has been examined in Drosophila melanogaster. The steady-state level of pol gamma -beta mRNA increases during the first hours of development, reaching its maximum value at the start of mtDNA replication in Drosophila embryos. In contrast, the steady-state level of pol gamma -alpha mRNA decreases as development proceeds and is low in stages of active mtDNA replication. This difference in mRNA abundance results at least in part from differences in the rates of mRNA synthesis. The pol gamma  genes are located in a compact cluster of five genes that contains three promoter regions (P1-P3). The P1 region directs divergent transcription of the pol gamma -beta gene and the adjacent rpII33 gene. P1 contains a DNA replication-related element (DRE) that is essential for pol gamma -beta promoter activity, but not for rpII33 promoter activity in Schneider's cells. A second divergent promoter region (P2) controls the expression of the orc5 and sop2 genes. The P2 region contains two DREs that are essential for orc5 promoter activity, but not for sop2 promoter activity. The expression of the pol gamma -alpha gene is directed by P3, a weak promoter that does not contain DREs. Electrophoretic mobility shift experiments demonstrate that the DRE-binding factor (DREF) regulatory protein binds to the DREs in P1 and P2. DREF regulates the expression of several genes encoding key factors involved in nuclear DNA replication. Its role in controlling the expression of the pol gamma -beta and orc5 genes establishes a common regulatory mechanism linking nuclear and mitochondrial DNA replication. Overall, our results suggest that the accessory subunit of mtDNA polymerase plays an important role in the control of mtDNA replication in Drosophila.

* This work was supported in part by Grant PB97-0034 (to R. G.) from the Direccion General de Enseñanza Superior, Ministerio de Educación y Ciencia, Spain and by Grant HL59656 (to L. S. K.) from the National Institutes of Health.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ These authors contributed equally to this work.

Recipient of a European Union fellowship from the Marie Curie Program.

** To whom correspondence should be addressed. Tel.: 34-91-3975452; Fax: 34-91-5854587; E-mail: rafael.garesse@uam.es.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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