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MBC in Press, published online ahead of print April 18, 2007
Mol. Biol. Cell 10.1091/mbc.E06-11-1033

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Submitted on November 22, 2006
Revised on April 4, 2007
Accepted on April 6, 2007

Developmental and Cell Cycle Regulation of the Drosophila Histone Locus Body

Anne E. White,* Michelle E. Leslie,{dagger} Brian R. Calvi,{ddagger} William F. Marzluff,*{dagger}{sect}|| and Robert J. Duronio*{dagger}||

*Department of Biology, {dagger}Curriculum in Genetics and Molecular Biology, {sect}Department of Biochemistry and Biophysics, and ||Program in Molecular Biology and Biotechnology, University of North Carolina, Chapel Hill, NC 27599; {ddagger}Department of Biology, Syracuse University, Syracuse, NY 13244

Monitoring Editor: Mark Solomon

Cyclin E/Cdk2 is necessary for replication-dependent histone mRNA biosynthesis, but how it controls this process in early development is unknown. We show that in Drosophila embryos the MPM-2 mAb, raised against a phosphoepitope from human mitotic cells, detects Cyclin E/Cdk2-dependent nuclear foci that colocalize with nascent histone transcripts. These foci are coincident with the histone locus body (HLB), a Cajal body-like nuclear structure associated with the histone locus and enriched in histone pre-mRNA processing factors such as Lsm11, a core component of the U7 snRNP. Using MPM-2 and anti-Lsm11 antibodies, we demonstrate that the HLB is absent in the early embryo and appears when zygotic histone transcription begins during nuclear cycle 11. Whereas the HLB is found in all cells after its formation, MPM-2 labels the HLB only in cells with active Cyclin E/Cdk2. MPM-2 and Lsm11 foci are present in embryos lacking the histone locus, and MPM-2 foci are present in U7 mutants, which cannot correctly process histone pre-mRNA. These data indicate that MPM-2 recognizes a Cdk2-regulated protein that assembles into the HLB independently of histone mRNA biosynthesis. HLB foci are present in histone deletion embryos, although the MPM-2 foci are smaller, and some Lsm11 foci are not associated with MPM-2 foci, suggesting that the histone locus is important for HLB integrity.

Address correspondence to: Robert J. Duronio (duronio{at}med.unc.edu)




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