Caenorhabditis elegans Heterochromatin protein 1 (HPL-2) links developmental plasticity, longevity and lipid metabolism.

Authors: Meister P; Schott S; Bedet C; Xiao Y; Rohner S; Bodennec S; Hudry B; Molin L; Solari F; Gasser SM; Palladino F

Abstract: BACKGROUND: Heterochromatin protein 1 (HP1) family proteins have a well-characterized role in heterochromatin packaging and gene regulation. Their function in organismal development, however, is less well understood. Here we used genome-wide expression profiling to assess novel functions of the Caenorhabditis elegans HP1 homolog HPL-2 at specific developmental stages. RESULTS: We show that HPL-2 regulates the expression of germline genes, extracellular matrix components and genes involved in lipid metabolism. Comparison of our expression data with HPL-2 ChIP-on-chip profiles reveals that a significant number of genes up- and down-regulated in the absence of HPL-2 are bound by HPL-2. Germline genes are specifically up-regulated in hpl-2 mutants, consistent with the function of HPL-2 as a repressor of ectopic germ cell fate. In addition, microarray results and phenotypic analysis suggest that HPL-2 regulates the dauer developmental decision, a striking example of phenotypic plasticity in which environmental conditions determine developmental fate. HPL-2 acts in dauer at least partly through modulation of daf-2/IIS and TGF-beta signaling pathways, major determinants of the dauer program. hpl-2 mutants also show increased longevity and altered lipid metabolism, hallmarks of the long-lived, stress resistant dauers. CONCLUSIONS: Our results suggest that the worm HP1 homologue HPL-2 may coordinately regulate dauer diapause, longevity and lipid metabolism, three processes dependent on developmental input and environmental conditions. Our findings are of general interest as a paradigm of how chromatin factors can both stabilize development by buffering environmental variation, and guide the organism through remodeling events that require plasticity of cell fate regulation.

Keywords: Animals; Caenorhabditis elegans/*genetics/growth & development/metabolism; Caenorhabditis elegans Proteins/*genetics/metabolism; Chromosomal Proteins, Non-Histone/*genetics/metabolism; Environment; Gene Expression Profiling; *Gene Expression Regulation, Developmental; Germ Cells/growth & development/metabolism; Hermaphroditic Organisms; Heterochromatin/genetics; Lipid Metabolism/*genetics; Longevity/*genetics; Male; Mutation; Oligonucleotide Array Sequence Analysis; Receptor, Insulin/genetics/metabolism; Repressor Proteins/*genetics/metabolism; Signal Transduction; Transforming Growth Factor beta/genetics/metabolism
Journal: Genome biology
Volume: 12
Issue: 12
Pages: R123
Date: Dec. 22, 2011
PMID: 22185090
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Citation:

Meister P, Schott S, Bedet C, Xiao Y, Rohner S, Bodennec S, Hudry B, Molin L, Solari F, Gasser SM, Palladino F (2011) Caenorhabditis elegans Heterochromatin protein 1 (HPL-2) links developmental plasticity, longevity and lipid metabolism. Genome biology 12: R123.


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