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Functional dissection of the Drosophila melanogaster condensin subunit Cap-G reveals its exclusive association with condensin I.

ABSTRACT: The heteropentameric condensin complexes have been shown to participate in mitotic chromosome condensation and to be required for unperturbed chromatid segregation in nuclear divisions. Vertebrates have two condensin complexes, condensin I and condensin II, which contain the same structural maintenance of chromosomes (SMC) subunits SMC2 and SMC4, but differ in their composition of non-SMC subunits. While a clear biochemical and functional distinction between condensin I and condensin II has been established in vertebrates, the situation in Drosophila melanogaster is less defined. Since Drosophila lacks a clear homolog for the condensin II-specific subunit Cap-G2, the condensin I subunit Cap-G has been hypothesized to be part of both complexes. In vivo microscopy revealed that a functional Cap-G-EGFP variant shows a distinct nuclear enrichment during interphase, which is reminiscent of condensin II localization in vertebrates and contrasts with the cytoplasmic enrichment observed for the other EGFP-fused condensin I subunits. However, we show that this nuclear localization is dispensable for Cap-G chromatin association, for its assembly into the condensin I complex and, importantly, for development into a viable and fertile adult animal. Immunoprecipitation analyses and complex formation studies provide evidence that Cap-G does not associate with condensin II-specific subunits, while it can be readily detected in complexes with condensin I-specific proteins in vitro and in vivo. Mass-spectrometric analyses of proteins associated with the condensin II-specific subunit Cap-H2 not only fail to identify Cap-G but also the other known condensin II-specific homolog Cap-D3. As condensin II-specific subunits are also not found associated with SMC2, our results question the existence of a soluble condensin II complex in Drosophila.

SUBMITTER: Herzog S

PROVIDER: S-EPMC3630105 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Functional dissection of the Drosophila melanogaster condensin subunit Cap-G reveals its exclusive association with condensin I.

Herzog Sabine S Nagarkar Jaiswal Sonal S Urban Evelin E Riemer Anna A Fischer Sina S Heidmann Stefan K SK

PLoS genetics 20130418 4

The heteropentameric condensin complexes have been shown to participate in mitotic chromosome condensation and to be required for unperturbed chromatid segregation in nuclear divisions. Vertebrates have two condensin complexes, condensin I and condensin II, which contain the same structural maintenance of chromosomes (SMC) subunits SMC2 and SMC4, but differ in their composition of non-SMC subunits. While a clear biochemical and functional distinction between condensin I and condensin II has been ...[more]

PMID: 23637630

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Project description:Retrotransposon sequences are positioned throughout the genome of almost every eukaryote that has been sequenced. As mobilization of these elements can have detrimental effects on the transcriptional regulation and stability of an organism's genome, most organisms have evolved mechanisms to repress their movement. Here, we identify a novel role for the Drosophila melanogaster Condensin II subunit, dCAP-D3 in preventing the mobilization of retrotransposons located in somatic cell euchromatin. dCAP-D3 regulates transcription of euchromatic gene clusters which contain or are proximal to retrotransposon sequence. ChIP experiments demonstrate that dCAP-D3 binds to these loci and is important for maintaining a repressed chromatin structure within the boundaries of the retrotransposon and for repressing retrotransposon transcription. We show that dCAP-D3 prevents accumulation of double stranded DNA breaks within retrotransposon sequence, and decreased dCAP-D3 levels leads to a precise loss of retrotransposon sequence at some dCAP-D3 regulated gene clusters and a gain of sequence elsewhere in the genome. Homologous chromosomes exhibit high levels of pairing in Drosophila somatic cells, and our FISH analyses demonstrate that retrotransposon-containing euchromatic loci are regions which are actually less paired than euchromatic regions devoid of retrotransposon sequences. Decreased dCAP-D3 expression increases pairing of homologous retrotransposon-containing loci in tissue culture cells. We propose that the combined effects of dCAP-D3 deficiency on double strand break levels, chromatin structure, transcription and pairing at retrotransposon-containing loci may lead to 1) higher levels of homologous recombination between repeats flanking retrotransposons in dCAP-D3 deficient cells and 2) increased retrotransposition. These findings identify a novel role for the anti-pairing activities of dCAP-D3/Condensin II and uncover a new way in which dCAP-D3/Condensin II influences local chromatin structure to help maintain genome stability.

Dataset Information

Functional dissection of the Drosophila melanogaster condensin subunit Cap-G reveals its exclusive association with condensin I.

Publications

Functional dissection of the Drosophila melanogaster condensin subunit Cap-G reveals its exclusive association with condensin I.

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