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Drosophila lipid droplets buffer the H2Av supply to protect early embryonic development.

ABSTRACT: Assembly of DNA into chromatin requires a delicate balancing act, as both dearth and excess of histones severely disrupt chromatin function [1-3]. In particular, cells need to carefully control histone stoichiometry: if different types of histones are incorporated into chromatin in an imbalanced manner, it can lead to altered gene expression, mitotic errors, and death [4-6]. Both the balance between individual core histones and the balance between core histones and histone variants are critical [5, 7]. Here, we find that in early Drosophila embryos, histone balance in the nuclei is regulated by lipid droplets, cytoplasmic fat-storage organelles [8]. Lipid droplets were previously known to function in long-term histone storage: newly laid embryos contain large amounts of excess histones generated during oogenesis [9], and the maternal supplies of core histone H2A and the histone variant H2Av are anchored to lipid droplets via the novel protein Jabba [3]. We find that in these embryos, synthesis of new H2A and H2Av is imbalanced, and that newly produced H2Av can be recruited to lipid droplets. When droplet sequestration is disrupted by mutating Jabba, embryos display an elevated H2Av/H2A ratio in nuclei as well as mitotic defects, reduced viability, and hypersensitivity to H2Av overexpression. We propose that in Drosophila embryos, lipid droplets serve as a histone buffer, not only storing maternal histones to support the early cell cycles but also transiently sequestering H2Av produced in excess and thus ensuring proper histone balance in the nucleus.

SUBMITTER: Li Z

PROVIDER: S-EPMC4122669 | biostudies-other | 2014 Jul

REPOSITORIES: biostudies-other

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Drosophila lipid droplets buffer the H2Av supply to protect early embryonic development.

Li Zhihuan Z Johnson Matthew R MR Ke Zhonghe Z Chen Lili L Welte Michael A MA

Current biology : CB 20140612 13

Assembly of DNA into chromatin requires a delicate balancing act, as both dearth and excess of histones severely disrupt chromatin function [1-3]. In particular, cells need to carefully control histone stoichiometry: if different types of histones are incorporated into chromatin in an imbalanced manner, it can lead to altered gene expression, mitotic errors, and death [4-6]. Both the balance between individual core histones and the balance between core histones and histone variants are critical ...[more]

PMID: 24930966

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Project description:Background:Calcium signaling are conserved from invertebrates to vertebrates and plays critical roles in many molecular mechanisms of embryogenesis and postnatal development. As a critical component of the signaling pathway, the RyR medicated calcium-induced calcium release signaling system, has been well studied along with their regulator FK506-binding protein 12 (FKBP12/Calstabin). Lack of FKBP12 is known to result in lethal cardiac dysfunction in mouse. However, precisely how FKBP12 is regulated and effects calcium signaling in Drosophila melanogaster remains largely unknown. Results:In this study, we identified both temporal and localization changes in expression of DmFKBP12, a translational and transcriptional regulator of Drosophila RyR (DmRyR) and FKBP12, through embryonic development. DmFKBP12 is first expressed at the syncytial blastoderm stage and undergoes increased expression during the cellular blastoderm and early gastrulation stages. At late gastrulation, DmFKBP12 expression begins to decline until it reaches homeostasis, which it then maintains throughout the rest of development. Throughout these described changes in expression, DmFKBP12 mRNA remain stable, which indicates that protein dynamics are attributed to regulation at the mRNA to protein translation level. In addition to temporal changes in expression, dynamic expression profiles during Drosophila development also revealed DmFKBP12 localization. Although DmFKBP12 is distributed evenly between the anterior to posterior poles of the blastoderm egg, the protein is expressed more strongly in the cortex of the early Drosophila gastrula with the highest concentration found in the basement membrane of the cellular blastoderm. Fertilized egg, through the profile as under-membrane cortex distribution concentering onto basement at cellular blastoderm, to the profile as three-gem layer localization in primitive neuronal and digestion architecture of early Drosophila gastrula. By late gastrulation, DmFKBP12 is no longer identified in the yolk or lumen of duct structures and has relocated to the future brain (suboesophageal and supraesophageal ganglions), ventral nervous system, and muscular system. Throughout these changes in distribution, in situ DmFKBP12 mRNA monitoring detected equal distribution of DmFKBP12 mRNA, once again indicating that regulation of DmFKBP12 occurs at the translational level in Drosophila development. Conclusion:As a critical regulator of the DmRyR-FKBP complex, DmFKBP12 expression in Drosophila fluctuates temporally and geographically with the formation of organ systems. These finding indicate that DmFKBP12 and RyR associated calcium signaling plays an essential role in the successful development of Drosophila melanogaster. Further study on the differences between mammalian RyR-FKBP12 and Drosophila DmRyR-FKBP12 can be exploited to develop safe pesticides.

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Drosophila lipid droplets buffer the H2Av supply to protect early embryonic development.

Publications

Drosophila lipid droplets buffer the H2Av supply to protect early embryonic development.

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