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J Biol Chem, Vol. 275, Issue 18, 13628-13636, May 5, 2000

Regulation of Mitochondrial Single-stranded DNA-binding Protein Gene Expression Links Nuclear and Mitochondrial DNA Replication in Drosophila*

Inmaculada Ruiz de MenaDagger §, Etienne Lefai§, Rafael Garesse§, and Laurie S. KaguniDagger ||

From the Dagger  Department of Biochemistry, Michigan State University, East Lansing, Michigan 48824-1319 and the § Instituto de Investigaciones Biomedicas Alberto Sols, Universidad Autónoma de Madrid-Consejo Superior de Investigaciones Científicas, Arturo Duperier 4, Madrid 28028, Spain

The structural organization of the Drosophila melanogaster gene encoding mitochondrial single-stranded DNA-binding protein (mtSSB) has been determined and its pattern of expression evaluated during Drosophila development. The D. melanogaster mtSSB gene contains four exons and three small introns. The transcriptional initiation site is located 22 nucleotides upstream from the initiator translation codon in adults, whereas several initiation sites are found in embryos. No consensus TATA or CAAT sequences are located at canonical positions, although an AT-rich sequence was identified flanking the major transcriptional initiation site. Northern analyses indicated that the mtSSB transcript is present at variable levels throughout development. In situ hybridization analysis shows that maternally deposited mtSSB mRNA is distributed homogeneously in the early embryo, whereas de novo transcript is produced specifically at an elevated level in the developing midgut. Transfection assays in cultured Schneider cells with promoter region deletion constructs revealed that the proximal 230 nucleotides contain cis-acting elements required for efficient gene expression. Putative transcription factor binding sites clustered within this region include two Drosophila DNA replication-related elements (DRE) and a single putative E2F binding site. Deletion and base substitution mutagenesis of the DRE sites demonstrated that they are required for efficient promoter activity, and gel electrophoretic mobility shift analyses showed that DRE binding factor (DREF) binds to these sites. Our data suggest strongly that the Drosophila mtSSB gene is regulated by the DRE/DREF system. This finding represents a first link between nuclear and mitochondrial DNA replication.

* This work was supported in part by National Institutes of Health Grants GM45295 and HL59656 (to L. S. K.), Grant PB94-0088 from the Ministerio de Educación y Ciencia, Spain, and European Union Human Capital and Mobility Program Network Grant CHRX-CT94-0494 (to R. G.).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.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) AF181084.

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

|| To whom correspondence should be addressed. Tel.: 517-353-6703; Fax: 517-353-9334; E-mail: lskaguni@pilot.msu.edu.

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