The SuUR gene influences the distribution of heterochromatic proteins HP1 and SU(VAR)3–9 on nurse cell polytene chromosomes of Drosophila melanogaster

Abstract

We have investigated the distribution of three heterochromatic proteins [SUppressor of UnderReplication (SUUR), heterochromatin protein 1 (HP1), and SU(VAR)3-9] in chromosomes of nurse cells (NCs) and have compared the data obtained with the distribution of the same proteins in salivary gland (SG) chromosomes. In NC chromosomes, the SU(VAR)3-9 protein was found in pericentric heterochromatin and at 223 sites on euchromatic arms, while in SG chromosomes, it was mainly restricted to the chromocenter. In NC chromosomes, the HP1 and SUUR proteins bind to 331 and 256 sites, respectively, which are almost twice the number of sites in SG chromosomes. The distribution of the HP1 and SU(VAR)3-9 proteins depends on the SuUR gene. A mutation in this gene results in a dramatic decrease in the amount of SU(VAR)3-9 binding sites in autosomes. In the X chromosome, these sites are relocated in comparison to the SuUR (+), and their total number only varies slightly. HP1 binding sites are redistributed in chromosomes of SuUR mutants, and their overall number did not change as considerably as SU(VAR)3-9. These data together point to an interaction of these three proteins in Drosophila NC chromosomes.

Heterochromatin protein 1 (HP1) modulates replication timing of the Drosophila genome

“…Interestingly, however, embryonic stem cells lacking the SUV39H1 and SUV39H2 H3K9 methyltransferases showed delayed replication timing of centromeric repeats (Jorgensen et al 2007), underscoring the context dependency of the interaction between chromatin and the replication timing program. Studies of endoreplication of Drosophila polytene chromosomes have suggested a role for HP1 in the maintenance of underreplicated regions in connection with the SuUR protein (Makunin et al 2002;Koryakov et al 2006;Pindyurin et al 2007Pindyurin et al , 2008. It has been suggested that open chromatin plays a role in replication initiation (Aggarwal and Calvi 2004;Goren et al 2008;Schwaiger et al 2009;Hansen et al 2010;Macalpine et al 2010).…”

“…Interestingly, in Drosophila polytene chromosomes and Kc cells, HP1 target regions often overlap with regions bound by the Suppressor of Underreplication (SuUR) protein (Koryakov et al 2006;Pindyurin et al 2007). SuUR binds to underreplicated and late replicating regions on Drosophila polytene chromosomes (Makunin et al 2002) and to late replicating regions in Kc cells (Pindyurin et al 2007).…”

DNA replication in nurse cell polytene chromosomes of Drosophila melanogaster otu mutants

“…Overall, in contrast to SGs (Zhimulev et al 1982), the frequency of chromosome breaks in NCs is remarkably low (Koryakov et al 2006). Of 42 such regions, only 24 correspond to late replication sites (Fig.…”

“…To compare positions of late-replicating regions and regions associated with SUUR, the data published previously were used (Koryakov et al 2006). We revised the list of SUURpositive chromosomal sites, and added several regions…”

“…Notably, pericentric heterochromatin is polytenized in otu NCs significantly more than in SG polytene chromosomes and may form structures with reproducible banding pattern (Mal'ceva and Zhimulev 1993;Koryakov et al 1996;1999;. Moreover, the degree of DNA underreplication and hence the frequency of chromosome breaks are much lower in intercalary heterochromatin regions of NC polytene chromosomes vs those of SGs (Mal'ceva et al 1995;Koryakov et al 2006).…”