Integration site selection by retroviruses and transposable elements in eukaryotes

Sultana, Tania; Zamborlini, Alessia; Cristofari, Gaël; Lesage, Pascale

doi:10.1038/nrg.2017.7

Cited by 223 publications

(253 citation statements)

References 210 publications

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“…However, our analysis does not rule out that LTR integration and inter-chromosomal rearrangement could co-occur in the same location without a causal relationship. Indeed, local genomic properties, such as chromatin structure are known hot spots for both transposable element integration and chromosomal breakpoints (Capilla et al 2016;Sultana et al 2017). In summary, our results detail a punctate event of chromosome reshuffling that happened in the Muridae lineage between 3 and 6 MYA and that has led to the observed karyotype of laboratory mice.…”

Section: Sequencing Assembly and Annotation Of Mus Caroli And Mus Pmentioning

confidence: 69%

Repeat associated mechanisms of genome evolution and function revealed by the Mus caroli and Mus pahari genomes

et al. 2018

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Understanding the mechanisms driving lineage-specific evolution in both primates and rodents has been hindered by the lack of sister clades with a similar phylogenetic structure having high-quality genome assemblies. Here, we have created chromosome-level assemblies of the Mus caroli and Mus pahari genomes. Together with the Mus musculus and Rattus norvegicus genomes, this set of rodent genomes is similar in divergence times to the Hominidae (human-chimpanzee-gorilla-orangutan). By comparing the evolutionary dynamics between the Muridae and Hominidae, we identified punctate events of chromosome reshuffling that shaped the ancestral karyotype of Mus musculus and Mus caroli between 3 and 6 million yr ago, but that are absent in the Hominidae. Hominidae show between four-and sevenfold lower rates of nucleotide change and feature turnover in both neutral and functional sequences, suggesting an underlying coherence to the Muridae acceleration. Our system of matched, high-quality genome assemblies revealed how specific classes of repeats can play lineage-specific roles in related species. Recent LINE activity has remodeled protein-coding loci to a greater extent across the Muridae than the Hominidae, with functional consequences at the species level such as reproductive isolation. Furthermore, we charted a Muridae-specific retrotransposon expansion at unprecedented resolution, revealing how a single nucleotide mutation transformed a specific SINE element into an active CTCF binding site carrier specifically in Mus caroli, which resulted in thousands of novel, species-specific CTCF binding sites. Our results show that the comparison of matched phylogenetic sets of genomes will be an increasingly powerful strategy for understanding mammalian biology.

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Section: Sequencing Assembly and Annotation Of Mus Caroli And Mus Pmentioning

confidence: 69%

Repeat associated mechanisms of genome evolution and function revealed by the Mus caroli and Mus pahari genomes

et al. 2018

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show abstract

“…Finally, it is worth stressing that the insertion sites of TEs are usually non‐random because some specific nucleotidic sequences, chromatin and nuclear contexts may partly guide the location of their de novo integration (Sultana et al ., ). This implies that environmentally induced epigenetic modifications may promote and guide the insertion of TEs into specifically targeted genomic regions.…”

Section: All Roads Lead To Genes Via the Epigenetic Hubmentioning

confidence: 97%

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

et al. 2018

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After decades of debate about the existence of non‐genetic inheritance, the focus is now slowly shifting towards dissecting its underlying mechanisms. Here, we propose a new mechanism that, by integrating non‐genetic and genetic inheritance, may help build the long‐sought inclusive vision of evolution. After briefly reviewing the wealth of evidence documenting the existence and ubiquity of non‐genetic inheritance in a table, we review the categories of mechanisms of parent–offspring resemblance that underlie inheritance. We then review several lines of argument for the existence of interactions between non‐genetic and genetic components of inheritance, leading to a discussion of the contrasting timescales of action of non‐genetic and genetic inheritance. This raises the question of how the fidelity of the inheritance system can match the rate of environmental variation. This question is central to understanding the role of different inheritance systems in evolution. We then review and interpret evidence indicating the existence of shifts from inheritance systems with low to higher transmission fidelity. Based on results from different research fields we propose a conceptual hypothesis linking genetic and non‐genetic inheritance systems. According to this hypothesis, over the course of generations, shifts among information systems allow gradual matching between the rate of environmental change and the inheritance fidelity of the corresponding response. A striking conclusion from our review is that documented shifts between types of inherited non‐genetic information converge towards epigenetics (i.e. inclusively heritable molecular variation in gene expression without change in DNA sequence). We then interpret the well‐documented mutagenicity of epigenetic marks as potentially generating a final shift from epigenetic to genetic encoding. This sequence of shifts suggests the existence of a relay in inheritance systems from relatively labile ones to gradually more persistent modes of inheritance, a relay that could constitute a new mechanistic basis for the long‐proposed, but still poorly documented, hypothesis of genetic assimilation. A profound difference between the genocentric and the inclusive vision of heredity revealed by the genetic assimilation relay proposed here lies in the fact that a given form of inheritance can affect the rate of change of other inheritance systems. To explore the consequences of such inter‐connection among inheritance systems, we briefly review published theoretical models to build a model of genetic assimilation focusing on the shift in the engraving of environmentally induced phenotypic variation into the DNA sequence. According to this hypothesis, when environmental change remains stable over a sufficient number of generations, the relay among inheritance systems has the potential to generate a form of genetic assimilation. In this hypothesis, epigenetics appears as a hub by which non‐genetically inherited environmentally induced variation in traits can be...

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“…The staggered cleavage of the target DNA molecule leads to target site duplications (TSDs), which are a hallmark of DDE integration. Although the rve‐INTs of some retroviruses have a weak sequence preference for short nonpalindromic DNA motifs, target site specificity is primarily determined by the interaction between the integrase and host chromatin binding proteins . Since particular retroviral integrases interact with different host proteins, the integration patterns within mammalian genomes vary among retroviruses .…”

Section: Virophages Encode Retroviral Integrases and Tyrosine Recombimentioning

confidence: 99%

The dual lifestyle of genome‐integrating virophages in protists

Berjón-Otero

Koslová

Fischer

2019

Annals of the New York Academy of Sciences

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DNA viruses with efficient host genome integration capability were unknown in eukaryotes until recently. The discovery of virophages, satellite‐like DNA viruses that depend on lytic giant viruses that infect protists, revealed a genetically diverse group of viruses with high genome mobility. Virophages can act as strong inhibitors of their associated giant viruses, and the resulting beneficial effects on their unicellular hosts resemble a population‐based antiviral defense mechanism. By comparing various aspects of genome‐integrating virophages, in particular the virophage mavirus, with other mobile genetic elements and parasite‐derived defense mechanisms in eukaryotes and prokaryotes, we show that virophages share many features with other host–parasite systems. Yet, the dual lifestyle exhibited by mavirus remains unprecedented among eukaryotic DNA viruses, with potentially far‐reaching ecological and evolutionary consequences for the host.

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Integration site selection by retroviruses and transposable elements in eukaryotes

Cited by 223 publications

References 210 publications

Repeat associated mechanisms of genome evolution and function revealed by the Mus caroli and Mus pahari genomes

Repeat associated mechanisms of genome evolution and function revealed by the Mus caroli and Mus pahari genomes

Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis

The dual lifestyle of genome‐integrating virophages in protists

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