TY - JOUR
T1 - Regulatory functions and chromatin loading dynamics of linker histone H1 during endoreplication in Drosophila
AU - Andreyeva, Evgeniya N.
AU - Bernardo, Travis J.
AU - Kolesnikova, Tatyana D.
AU - Lu, Xingwu
AU - Yarinich, Lyubov A.
AU - Bartholdy, Boris A.
AU - Guo, Xiaohan
AU - Posukh, Olga V.
AU - Healton, Sean
AU - Willcockson, Michael A.
AU - Pindyurin, Alexey V.
AU - Zhimulev, Igor F.
AU - Skoultchi, Arthur I.
AU - Fyodorov, Dmitry V.
N1 - Funding Information:
We are grateful to Harald Saumweber and Giorgia Siriaco for antibodies and fly stocks. We thank Elena Vershilova for expert technical assistance, and Elena Belyaeva for help with chromosome break frequency scoring. We also thank Elena Belyaeva and members of the Pindyurin, Zhimulev, Skoultchi, and Fyo-dorov laboratories for critical reading of the manuscript and valuable suggestions. Antibodies were raised at the Center for Genetic Resources of Laboratory Animals, Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences (RFMEFI61914X0005 and RFMEFI61914X0010). This work was supported by grants from the National Institutes of Health (NIH) to A.I.S. (GM093190 and GM116143) and D.V.F. (GM074233), a Cancer Center Support grant from the NIH to Albert Einstein College of Medicine (CA013330), a grant from the Russian Fundamental Scientific Research Project to I.F.Z. (0310-2016-0005), a Russian Foundation for Basic Research grant to A.V.P. (16-04-01598), and a grant from the Russian Science Foundation to A.V.P (16-14-10288). T.J.B. was supported in part by NIH F32 Fellowship (GM115210) and the NIH Institutional Research and Academic Career Development Award/K12 training grant (GM1027779). S.H. and M.A.W. were supported in part by NIH F30 Fellowships (CA210539 and DK107182, respectively).
Funding Information:
We are grateful to Harald Saumweber and Giorgia Siriaco for antibodies and fly stocks. We thank Elena Vershilova for expert technical assistance, and Elena Belyaeva for help with chromosome break frequency scoring. We also thank Elena Belyaeva and members of the Pindyurin, Zhimulev, Skoultchi, and Fyodorov laboratories for critical reading of the manuscript and valuable suggestions. Antibodies were raised at the Center for Genetic Resources of Laboratory Animals, Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences (RFMEFI61914X0005 and RFMEFI61914X0010). This work was supported by grants from the National Institutes of Health (NIH) to A.I.S. (GM093190 and GM116143) and D.V.F. (GM074233), a Cancer Center Support grant from the NIH to Albert Einstein College of Medicine (CA013330), a grant from the Russian Fundamental Scientific Research Project to I.F.Z. (0310-2016-0005), a Russian Foundation for Basic Research grant to A.V.P. (16-04-01598), and a grant from the Russian Science Foundation to A.V.P (16-14-10288). T.J.B. was supported in part by NIH F32 Fellowship (GM115210) and the NIH Institutional Research and Academic Career Development Award/K12 training grant (GM1027779). S.H. and M.A.W. were supported in part by NIH F30 Fellowships (CA210539 and DK107182, respectively).
Publisher Copyright:
© 2017 Andreyeva et al.
PY - 2017
Y1 - 2017
N2 - Eukaryotic DNA replicates asynchronously, with discrete genomic loci replicating during different stages of S phase. Drosophila larval tissues undergo endoreplication without cell division, and the latest replicating regions occasionally fail to complete endoreplication, resulting in underreplicated domains of polytene chromosomes. Here we show that linker histone H1 is required for the underreplication (UR) phenomenon in Drosophila salivary glands. H1 directly interacts with the Suppressor of UR (SUUR) protein and is required for SUUR binding to chromatin in vivo. These observations implicate H1 as a critical factor in the formation of underreplicated regions and an upstream effector of SUUR. We also demonstrate that the localization of H1 in chromatin changes profoundly during the endocycle. At the onset of endocycle S (endo-S) phase, H1 is heavily and specifically loaded into late replicating genomic regions and is then redistributed during the course of endoreplication. Our data suggest that cell cycle-dependent chromosome occupancy of H1 is governed by several independent processes. In addition to the ubiquitous replication-related disassembly and reassembly of chromatin, H1 is deposited into chromatin through a novel pathway that is replication-independent, rapid, and locus-specific. This cell cycle-directed dynamic localization of H1 in chromatin may play an important role in the regulation of DNA replication timing.
AB - Eukaryotic DNA replicates asynchronously, with discrete genomic loci replicating during different stages of S phase. Drosophila larval tissues undergo endoreplication without cell division, and the latest replicating regions occasionally fail to complete endoreplication, resulting in underreplicated domains of polytene chromosomes. Here we show that linker histone H1 is required for the underreplication (UR) phenomenon in Drosophila salivary glands. H1 directly interacts with the Suppressor of UR (SUUR) protein and is required for SUUR binding to chromatin in vivo. These observations implicate H1 as a critical factor in the formation of underreplicated regions and an upstream effector of SUUR. We also demonstrate that the localization of H1 in chromatin changes profoundly during the endocycle. At the onset of endocycle S (endo-S) phase, H1 is heavily and specifically loaded into late replicating genomic regions and is then redistributed during the course of endoreplication. Our data suggest that cell cycle-dependent chromosome occupancy of H1 is governed by several independent processes. In addition to the ubiquitous replication-related disassembly and reassembly of chromatin, H1 is deposited into chromatin through a novel pathway that is replication-independent, rapid, and locus-specific. This cell cycle-directed dynamic localization of H1 in chromatin may play an important role in the regulation of DNA replication timing.
KW - Endoreplication
KW - Intercalary heterochromatin]
KW - Linker histone H1
KW - Polytene chromosomes
KW - Replication timing
KW - Suppressor of underreplication
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U2 - 10.1101/gad.295717.116
DO - 10.1101/gad.295717.116
M3 - Article
C2 - 28404631
AN - SCOPUS:85018609301
SN - 0890-9369
VL - 31
SP - 603
EP - 616
JO - Genes and Development
JF - Genes and Development
IS - 6
ER -