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Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells.

Arico JK, Katz DJ, van der Vlag J, Kelly WG - PLoS Genet. (2011)

Bottom Line: Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring.These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content.This content can be maintained and may heritably affect gene expression in the offspring.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, Rollins Research Center, Emory University, Atlanta, Georgia, United States of America.

ABSTRACT
Epigenetic information, such as parental imprints, can be transmitted with genetic information from parent to offspring through the germ line. Recent reports show that histone modifications can be transmitted through sperm as a component of this information transfer. How the information that is transferred is established in the parent and maintained in the offspring is poorly understood. We previously described a form of imprinted X inactivation in Caenorhabditis elegans where dimethylation on histone 3 at lysine 4 (H3K4me2), a mark of active chromatin, is excluded from the paternal X chromosome (Xp) during spermatogenesis and persists through early cell divisions in the embryo. Based on the observation that the Xp (unlike the maternal X or any autosome) is largely transcriptionally inactive in the paternal germ line, we hypothesized that transcriptional activity in the parent germ line may influence epigenetic information inherited by and maintained in the embryo. We report that chromatin modifications and histone variant patterns assembled in the germ line can be retained in mature gametes. Furthermore, despite extensive chromatin remodeling events at fertilization, the modification patterns arriving with the gametes are largely retained in the early embryo. Using transgenes, we observe that expression in the parental germline correlates with differential chromatin assembly that is replicated and maintained in the early embryo. Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring. These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content. This content can be maintained and may heritably affect gene expression in the offspring.

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Mature sperm chromatin retains epigenetic information established in meiosis.Antibody staining for H3.3::GFP, H3.1 and H3K4me0 compared to antibody staining for H3K4me2 in mature hermaphrodite spermatids. (A) H3.3::GFP has substantial overlap with H3K4me2, but is depleted from the X region (arrow), which lacks H3K4me2. In contrast, both H3.1(B) and H3K4me0 (C) are enriched on the X chromosome, marked by a lack of H3K4me2 (arrows). Antibodies (green) with DAPI (red). Scale bars, 5 um. (D) H3 is abundant in mature sperm chromatin at levels near that of embryonic chromatin by western blot analysis. Lanes were loaded with DNA equivalents as indicated. 1) embryo 1X DNA, 2) embryo 2X DNA, 3) sperm 1X DNA, 4) sperm 2X DNA.
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pgen-1001391-g003: Mature sperm chromatin retains epigenetic information established in meiosis.Antibody staining for H3.3::GFP, H3.1 and H3K4me0 compared to antibody staining for H3K4me2 in mature hermaphrodite spermatids. (A) H3.3::GFP has substantial overlap with H3K4me2, but is depleted from the X region (arrow), which lacks H3K4me2. In contrast, both H3.1(B) and H3K4me0 (C) are enriched on the X chromosome, marked by a lack of H3K4me2 (arrows). Antibodies (green) with DAPI (red). Scale bars, 5 um. (D) H3 is abundant in mature sperm chromatin at levels near that of embryonic chromatin by western blot analysis. Lanes were loaded with DNA equivalents as indicated. 1) embryo 1X DNA, 2) embryo 2X DNA, 3) sperm 1X DNA, 4) sperm 2X DNA.

Mentions: Histone variant H3.3 incorporation correlates with transcriptionally active chromatin and other modes of chromatin remodeling, and is reported to be enriched on the XY body and unpaired chromatin targeted by MSCI in mammals [30], [31]. In contrast, and as previously reported, a C. elegans H3.3::GFP (HIS-72::GFP (zuIs178)) expressed in germ cells is largely absent from the X but accumulates on the autosomes in pachytene nuclei during both oogenesis and spermatogenesis in C. elegans [32]. Additionally, HIS-72::GFP accumulates on the X in mature oocytes ([32] and Figure 2B–2D). HIS-72::GFP is known to be present in haploid spermatids and thus survives sperm chromatin condensation [32]. We further observed, however, that whereas the rest of the chromosomes contain H3.3 in mature sperm, the X remains devoid of this variant (Figure 3A). The genomic distribution of H3.3 within sperm chromatin thus grossly overlaps with the general pattern of its distribution during gametogenesis.


Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells.

Arico JK, Katz DJ, van der Vlag J, Kelly WG - PLoS Genet. (2011)

Mature sperm chromatin retains epigenetic information established in meiosis.Antibody staining for H3.3::GFP, H3.1 and H3K4me0 compared to antibody staining for H3K4me2 in mature hermaphrodite spermatids. (A) H3.3::GFP has substantial overlap with H3K4me2, but is depleted from the X region (arrow), which lacks H3K4me2. In contrast, both H3.1(B) and H3K4me0 (C) are enriched on the X chromosome, marked by a lack of H3K4me2 (arrows). Antibodies (green) with DAPI (red). Scale bars, 5 um. (D) H3 is abundant in mature sperm chromatin at levels near that of embryonic chromatin by western blot analysis. Lanes were loaded with DNA equivalents as indicated. 1) embryo 1X DNA, 2) embryo 2X DNA, 3) sperm 1X DNA, 4) sperm 2X DNA.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3111476&req=5

pgen-1001391-g003: Mature sperm chromatin retains epigenetic information established in meiosis.Antibody staining for H3.3::GFP, H3.1 and H3K4me0 compared to antibody staining for H3K4me2 in mature hermaphrodite spermatids. (A) H3.3::GFP has substantial overlap with H3K4me2, but is depleted from the X region (arrow), which lacks H3K4me2. In contrast, both H3.1(B) and H3K4me0 (C) are enriched on the X chromosome, marked by a lack of H3K4me2 (arrows). Antibodies (green) with DAPI (red). Scale bars, 5 um. (D) H3 is abundant in mature sperm chromatin at levels near that of embryonic chromatin by western blot analysis. Lanes were loaded with DNA equivalents as indicated. 1) embryo 1X DNA, 2) embryo 2X DNA, 3) sperm 1X DNA, 4) sperm 2X DNA.
Mentions: Histone variant H3.3 incorporation correlates with transcriptionally active chromatin and other modes of chromatin remodeling, and is reported to be enriched on the XY body and unpaired chromatin targeted by MSCI in mammals [30], [31]. In contrast, and as previously reported, a C. elegans H3.3::GFP (HIS-72::GFP (zuIs178)) expressed in germ cells is largely absent from the X but accumulates on the autosomes in pachytene nuclei during both oogenesis and spermatogenesis in C. elegans [32]. Additionally, HIS-72::GFP accumulates on the X in mature oocytes ([32] and Figure 2B–2D). HIS-72::GFP is known to be present in haploid spermatids and thus survives sperm chromatin condensation [32]. We further observed, however, that whereas the rest of the chromosomes contain H3.3 in mature sperm, the X remains devoid of this variant (Figure 3A). The genomic distribution of H3.3 within sperm chromatin thus grossly overlaps with the general pattern of its distribution during gametogenesis.

Bottom Line: Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring.These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content.This content can be maintained and may heritably affect gene expression in the offspring.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, Rollins Research Center, Emory University, Atlanta, Georgia, United States of America.

ABSTRACT
Epigenetic information, such as parental imprints, can be transmitted with genetic information from parent to offspring through the germ line. Recent reports show that histone modifications can be transmitted through sperm as a component of this information transfer. How the information that is transferred is established in the parent and maintained in the offspring is poorly understood. We previously described a form of imprinted X inactivation in Caenorhabditis elegans where dimethylation on histone 3 at lysine 4 (H3K4me2), a mark of active chromatin, is excluded from the paternal X chromosome (Xp) during spermatogenesis and persists through early cell divisions in the embryo. Based on the observation that the Xp (unlike the maternal X or any autosome) is largely transcriptionally inactive in the paternal germ line, we hypothesized that transcriptional activity in the parent germ line may influence epigenetic information inherited by and maintained in the embryo. We report that chromatin modifications and histone variant patterns assembled in the germ line can be retained in mature gametes. Furthermore, despite extensive chromatin remodeling events at fertilization, the modification patterns arriving with the gametes are largely retained in the early embryo. Using transgenes, we observe that expression in the parental germline correlates with differential chromatin assembly that is replicated and maintained in the early embryo. Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring. These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content. This content can be maintained and may heritably affect gene expression in the offspring.

Show MeSH
Related in: MedlinePlus