piRNA dynamics in divergent zebrafish strains reveal long-lasting maternal influence on zygotic piRNA profiles

Kaaij, Lucas J.T.; Hoogstrate, Suzanne W.; Berezikov, Eugène; Ketting, René F.

doi:10.1261/rna.036400.112

Cited by 15 publications

(17 citation statements)

References 40 publications

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“…Analysis of piRNA populations in zebrafish hybrids show evidence for maternal effects on the ratio of sense and antisense piRNAs in the progeny (Kaaij et al, 2013). Despite similarities between the fly and zebrafish piRNA pathways, including presence of a pingpong loop and observed fertility phenotypes (Houwing et al, 2007(Houwing et al, , 2008, further investigation will be needed to determine the extent of inheritance in this system.…”

Section: Pirna Functions Beyond Transposon Silencingmentioning

confidence: 99%

piRNAs: from biogenesis to function

2014

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Distinguishing self from non-self plays a crucial role in safeguarding the germlines of metazoa from mobile DNA elements. Since their discovery less than a decade ago, Piwi-interacting RNAs ( piRNAs) have been shown to repress transposable elements in the germline and, hence, have been at the forefront of research aimed at understanding the mechanisms that maintain germline integrity. More recently, roles for piRNAs in gene regulation have emerged. In this Review, we highlight recent advances made in understanding piRNA function, highlighting the divergent nature of piRNA biogenesis in different organisms, and discussing the mechanisms of piRNA action during transcriptional regulation and in transgenerational epigenetic inheritance.

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Section: Pirna Functions Beyond Transposon Silencingmentioning

confidence: 99%

piRNAs: from biogenesis to function

2014

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“…Indeed, there was significantly higher piRNA expression from PERLs, and this phenomenon was consistently found in piRNA populations across development ( Figure 6E). Interestingly, PERLs were also enriched significantly for retro-transposons, which are the major piRNA targets in zebrafish (Houwing et al, 2007;Kaaij et al, 2013), but not DNA transposons ( Figure 6F and G). Given that DNA transposons cover a significantly larger fraction of the genome than retro-elements (Howe et al, 2013) this could indicate that retro-elements play a role in driving PERL expression.…”

Section: Perls Are Transposon-rich Pirna Producing Locimentioning

confidence: 99%

“…We described before that piRNAs, in particular those that are Ziwi-bound, are maternally provided to zebrafish embryos and can influence piRNA characteristics trans-generationally (Houwing et al, 2007;Kaaij et al, 2013). However, due to experimental difficulties in manipulating this maternal piRNA pool, the function of the maternal piRNAs in zebrafish is still unclear.…”

Section: Pirna Pathway Activation In Zebrafish Pgcsmentioning

confidence: 99%

Extensive nuclear gyration and pervasive non-genic transcription during primordial germ cell development in zebrafish

Redl

Domingues

Möckel³

et al. 2020

Preprint

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Primordial germ cells (PGCs) are the precursors of germ cells, which migrate to the genital ridge during early development. Relatively little is known about PGCs after their migration.We studied this post-migratory stage using microscopy and sequencing techniques, and found that many PGC-specific genes, including genes known to induce PGC fate in the mouse, are only activated several days after migration. At this same timepoint, PGC nuclei become extremely gyrated, displaying general opening of chromatin and high levels of transcription. This is accompanied by changes in nuage morphology, expression of large loci, named PERLs, enriched for retro-transposons and piRNAs, and a rise in piRNA biogenesis signatures.Interestingly, no nuclear Piwi protein could be detected at any timepoint, indicating that the zebrafish piRNA pathway is fully cytoplasmic. Our data show that the post-migratory stage of zebrafish PGCs holds many cues to both germ cell fate establishment and piRNA pathway activation.

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“…Long-term piRNA inheritance appears to be well conserved: recently it was shown that piRNAs are inherited for 50 generations in Drosophila [40], and for at least two generations in Danio rerio [44]. While piRNAs are involved in many inherited immunity effects, they are obviously not central to all such mechanisms.…”

Section: Inherited Protection Against Transposonsmentioning

confidence: 99%

Guest list or black list: heritable small RNAs as immunogenic memories

Rechavi

2014

Trends in Cell Biology

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Small RNA-mediated gene silencing plays a pivotal role in genome immunity by recognizing and eliminating viruses and transposons which otherwise may colonize the genome. However, this can be challenging since individual genomic parasites are highly diverse, and employ multiple immune evasion techniques. In this review, I discuss a new theory proposing that the integrity of the germline is maintained by transgenerationally-transmitted RNA "memories" that record ancestral gene expression patterns, and delineate "Self" from "Foreign" sequences. To maintain such recollection two tactics are employed in parallel: "black listing" of invading nucleic acids, and "guest listing" of endogenous genes. Studies in a number of organisms have shown that this memorization is used by the next generation small RNAs to act as "Inherited Vaccines" that ambush invading elements, or as "Inherited Licenses" that grant the transcription of autogenous sequences. KeywordsSmall RNA; Transgenerational Inheritance; Inherited Immunity; Self Vs. Non-Self; "Inherited Vaccines" Overview of transgenerational inheritanceEvolution progresses through an interplay between two major forces, selection and variation. Since the formulation of the Modern Synthesis the theory holds that the environment is limited in its contribution to the evolutionary course of action -it affects selection, but not the degree of variation [1,2]. However, recent discoveries in epigenetics suggest that the environment may influence variability as well [1]. If the parental environment is predictive of the conditions that the progeny will face (often for sessile or short-lived organisms), epigenetic responses can change the output of the encoded genetic information in an adaptive manner [3]. For example, the water flea Daphnia changes its normal developmental course and develops a "helmet" that protects it from predators, if it is born to a mother that survived a similar attack [4].Correspondence to: odedrechavi@gmail.com. Over the years, controversy surrounded the study of environmentally affected transgenerational inheritance. Today, an improved understanding of epigenetic mechanisms at the molecular level has provided a logical background to explain how, heretically, an adaptive acquired trait could become heritable [5]. Several epigenetic mechanisms could regulate the expression of relevant genes during transgenerational inheritance including DNA methylation, histone modification, and transmission of regulatory RNAs. Moreover, in many organisms, these pathways appear to be interconnected [5][6][7][8]. Europe PMC Funders GroupThis review will concentrate on recent discoveries that establish a role for small RNAs in transgenerational transmission of acquired defense. Furthermore, exciting examples of RNA-mediated non-Mendelian genetic effects will be discussed, along with their possible implications for the study of evolution and immunology. RNA-mediated gene silencing and inheritanceSince the original discovery that small RNAs derived from exogenously-provided dou...

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piRNA dynamics in divergent zebrafish strains reveal long-lasting maternal influence on zygotic piRNA profiles

Cited by 15 publications

References 40 publications

piRNAs: from biogenesis to function

piRNAs: from biogenesis to function

Extensive nuclear gyration and pervasive non-genic transcription during primordial germ cell development in zebrafish

Guest list or black list: heritable small RNAs as immunogenic memories

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