Retrotransposon Silencing by DNA Methylation Can Drive Mammalian Genomic Imprinting

Suzuki, Shunsuke; Ono, Ryuichi; Narita, Takanori; Pask, Andrew J; Shaw, Geoff; Wang, Changshan; Kohda, Takashi; Alsop, Amber E.; Graves, Jennifer A. Marshall; Kohara, Yuji; Ishino, Fumitoshi; Renfree, Marilyn B.; Kaneko-Ishino, Tomoko

doi:10.1371/journal.pgen.0030055

Cited by 191 publications

(198 citation statements)

References 33 publications

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“…Together with the reported absence of PEG10 in the platypus (prototheria) (31), this suggests that a Ty3-Gypsy retrotransposon integrated into the genome of a therian ancestor after the split from the prototherians and subsequently lost its mobility. The conservation of the frameshift elements as well as both ORFs strongly suggests that the remaining protein acquired a functional importance and supports a prediction that as well as the short ORF1 protein, a full-length fusion protein is generated.…”

Section: Resultsmentioning

confidence: 76%

Mammalian Gene PEG10 Expresses Two Reading Frames by High Efficiency –1 Frameshifting in Embryonic-associated Tissues

Clark¹,

Jänicke²,

Gottesbühren³

et al. 2007

Journal of Biological Chemistry

113

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Paternally expressed gene 10 (PEG10) is a mammalian gene that is essential for embryonic development in mice. The gene contains two overlapping open reading frames (ORF1 and ORF2) and is derived from a retroelement that acquired a cellular function. It is not known if both reading frames are required for PEG10 function. Synthesis of ORF2 would be possible only if programmed ؊1 frameshifting occurred during ORF1 translation. In this study the frameshifting activity of PEG10 was analyzed in vivo, and a potential role for ORF2 was investigated. Phylogenetic analysis demonstrated that PEG10 is highly conserved in therian mammals, with all species retaining the elements necessary for frameshifting as well as functional motifs in each ORF. The frameshift site of PEG10 was highly active in cultured cells and produced the ORF1-2 protein. In mice, endogenous ORF1 and an ORF1-2 frameshift protein were detected in the developing placenta and amniotic membrane from 9.5 days post-coitus through to term with a very high frameshift efficiency (>60%). Mutagenesis of the active site motif of a putative protease within ORF2 showed that this enzyme is active and participates in post-translational processing of PEG10 ORF1-2. Both PEG10 proteins were also detected in first trimester human placenta. By contrast, neither protein expression nor frameshifting was detected in adult mouse tissues. These studies imply that the ORF1-2 protein, synthesized utilizing the most efficient ؊1 frameshift mechanism yet documented in vivo, will have an essential function that is intrinsic to the importance of PEG10 in mammals.

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Section: Resultsmentioning

confidence: 76%

Mammalian Gene PEG10 Expresses Two Reading Frames by High Efficiency –1 Frameshifting in Embryonic-associated Tissues

Clark¹,

Jänicke²,

Gottesbühren³

et al. 2007

Journal of Biological Chemistry

113

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“…Genomic imprinting is an epigenetic phenomenon that results in monoallelic gene expression. In the vertebrates, imprinting seems to have evolved recently and has only been confirmed in marsupials and eutherian mammals 61,62 . The autosomal localization of some imprinted orthologues in platypus is known 63 .…”

Section: Samples It Is Now Known That Platypus Venom Is a Cocktail Omentioning

confidence: 99%

Genome analysis of the platypus reveals unique signatures of evolution

Warren¹,

Hillier²,

Graves³

et al. 2008

Nature

606

327

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A list of authors and their affiliations appears at the end of the paperWe present a draft genome sequence of the platypus, Ornithorhynchus anatinus. This monotreme exhibits a fascinating combination of reptilian and mammalian characters. For example, platypuses have a coat of fur adapted to an aquatic lifestyle; platypus females lactate, yet lay eggs; and males are equipped with venom similar to that of reptiles. Analysis of the first monotreme genome aligned these features with genetic innovations. We find that reptile and platypus venom proteins have been co-opted independently from the same gene families; milk protein genes are conserved despite platypuses laying eggs; and immune gene family expansions are directly related to platypus biology. Expansions of protein, non-protein-coding RNA and microRNA families, as well as repeat elements, are identified. Sequencing of this genome now provides a valuable resource for deep mammalian comparative analyses, as well as for monotreme biology and conservation.

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“…If so, genomic imprinting in the endosperm is likely a consequence of a mechanism destined to silence invading foreign DNA in the embryo. Similarly, the host defense hypothesis suggested that genomic imprinting in mammals evolved from existing mechanisms destined to silence foreign DNA elements (Barlow, 1993) and substantial supportive evidence for this hypothesis has been obtained recently (Suzuki et al, 2007;Pask et al, 2009). Figure 1 Reprogramming of epigenetic marks in gametes.…”

Section: Evolution Of the Imprinting Mechanism In The Endospermmentioning

confidence: 89%