scholarly journals Environmentally-Induced Transgenerational Epigenetic Inheritance: Implication of PIWI Interacting RNAs

Cells ◽  
2019 ◽  
Vol 8 (9) ◽  
pp. 1108 ◽  
Author(s):  
Karine Casier ◽  
Antoine Boivin ◽  
Clément Carré ◽  
Laure Teysset

Environmentally-induced transgenerational epigenetic inheritance is an emerging field. The understanding of associated epigenetic mechanisms is currently in progress with open questions still remaining. In this review, we present an overview of the knowledge of environmentally-induced transgenerational inheritance and associated epigenetic mechanisms, mainly in animals. The second part focuses on the role of PIWI-interacting RNAs (piRNAs), a class of small RNAs involved in the maintenance of the germline genome, in epigenetic memory to put into perspective cases of environmentally-induced transgenerational inheritance involving piRNA production. Finally, the last part addresses how genomes are facing production of new piRNAs, and from a broader perspective, how this process might have consequences on evolution and on sporadic disease development.

2015 ◽  
Vol 6 (2) ◽  
pp. 87-103 ◽  
Author(s):  
Abhay Sharma

AbstractTransgenerational epigenetic inheritance in animals has increasingly been reported in recent years. Controversies, however, surround this unconventional mode of heredity, especially in mammals, for several reasons. First, its existence itself has been questioned due to perceived insufficiency of available evidence. Second, it potentially implies transfer of hereditary information from soma to germline, against the established principle in biology. Third, it inherently requires survival of epigenetic memory across reprogramming, posing another fundamental challenge in biology. Fourth, evolutionary significance of epigenetic inheritance has also been under debate. This article pointwise addresses all these concerns on the basis of recent empirical, theoretical and conceptual advances. 1) Described here in detail are the key experimental findings demonstrating the occurrence of germline epigenetic inheritance in mammals. 2) Newly emerging evidence supporting soma to germline communication in transgenerational inheritance in mammals, and a role of exosome and extracellular microRNA in this transmission, is thoroughly discussed. 3) The plausibility of epigenetic information propagation across reprogramming is highlighted. 4) Analyses supporting evolutionary significance of epigenetic inheritance are briefly mentioned. Finally, an integrative model of ‘evolutionary transgenerational systems biology’ is proposed to provide a framework to guide future advancements in epigenetic inheritance.


2018 ◽  
Author(s):  
Yi Jin Liew ◽  
Emily J. Howells ◽  
Xin Wang ◽  
Craig T. Michell ◽  
John A. Burt ◽  
...  

MainThe notion that intergenerational or transgenerational inheritance operates solely through genetic means is slowly being eroded: epigenetic mechanisms have been shown to induce heritable changes in gene activity in plants1,2and metazoans1,3. Inheritance of DNA methylation provides a potential pathway for environmentally induced phenotypes to contribute to evolution of species and populations1–4. However, in basal metazoans, it is unknown whether inheritance of CpG methylation patterns occurs across the genome (as in plants) or as rare exceptions (as in mammals)4. Here, we demonstrate genome-wide intergenerational transmission of CpG methylation patterns from parents to sperm and larvae in a reef-building coral. We also show variation in hypermethylated genes in corals from distinct environments, indicative of responses to variations in temperature and salinity. These findings support a role of DNA methylation in the transgenerational inheritance of traits in corals, which may extend to enhancing their capacity to adapt to climate change.


2020 ◽  
Vol 48 (3) ◽  
pp. 1019-1034 ◽  
Author(s):  
Rachel M. Woodhouse ◽  
Alyson Ashe

Gene regulatory information can be inherited between generations in a phenomenon termed transgenerational epigenetic inheritance (TEI). While examples of TEI in many animals accumulate, the nematode Caenorhabditis elegans has proven particularly useful in investigating the underlying molecular mechanisms of this phenomenon. In C. elegans and other animals, the modification of histone proteins has emerged as a potential carrier and effector of transgenerational epigenetic information. In this review, we explore the contribution of histone modifications to TEI in C. elegans. We describe the role of repressive histone marks, histone methyltransferases, and associated chromatin factors in heritable gene silencing, and discuss recent developments and unanswered questions in how these factors integrate with other known TEI mechanisms. We also review the transgenerational effects of the manipulation of histone modifications on germline health and longevity.


2020 ◽  
Vol 7 ◽  
Author(s):  
Raquel Santana da Cruz ◽  
Elaine Chen ◽  
Megan Smith ◽  
Jaedus Bates ◽  
Sonia de Assis

2015 ◽  
Vol 2 (1) ◽  
Author(s):  
Marta Robertson ◽  
Christina Richards

AbstractEmerging evidence points to a causal role for epigenetic variation in evolution, but evolutionary biologists have been reluctant to incorporate epigenetics into modern evolutionary theory. Part of this ambivalence comes from the assumption that epigenetic inheritance is only relevant to the evolution of plants, which is perpetuated by a comparative lack of evolutionary studies in animals. However, although most of the evidence for epigenetic inheritance comes from plants, plants and animals share many homologous epigenetic mechanisms, and plants provide a more tractable system for investigating the causal role of epigenetic mechanisms underlying phenotypic variation and its relationship with fitness. The insights from studies of epigenetic inheritance in plants may be applicable across a broad range of taxa once we establish commonalities and differences in epigenetic machinery. In this paper we present evidence for a role of epigenetic mechanisms in the evolutionary process and discuss common objections to incorporating epigenetics into evolutionary theory. This review is not exhaustive, but is meant to demonstrate that epigenetic inheritance can be incorporated into current evolutionary theory without overhauling its foundations.


2018 ◽  
Author(s):  
Nora K E Schulz ◽  
Maike F Diddens-de Buhr ◽  
Joachim Kurtz

AbstractTrans-generational effects from fathers to offspring are increasingly reported from diverse organisms, but the underlying mechanisms are often unknown. Paternal trans-generational immune priming (TGIP) was demonstrated in the red flour beetle Tribolium castaneum: non-infectious bacterial exposure (priming) of fathers protects their offspring against an infectious challenge. Here we studied a potential role of the Dnmt2 (now also called Trdnmt1) gene, which encodes a highly conserved enzyme that provides CpG methylation to a set of tRNAs and has previously been reported to be involved in transgenerational epigenetic inheritance in mice. We first studied gene expression and found that Dnmt2 was expressed throughout life, with high expression in testes. Knockdown of Dnmt2 in fathers slowed down offspring larval development and increased mortality of the adult offspring upon bacterial infection. However, the observed effects were independent of the paternal priming treatment. In conclusion, our results point towards a role of Dnmt2 for paternal effects, while elucidation of the mechanisms behind paternal TGIP needs further studies.


2019 ◽  
Vol 53 (1) ◽  
pp. 289-311 ◽  
Author(s):  
Natasha E. Weiser ◽  
John K. Kim

In animals, small noncoding RNAs that are expressed in the germline and transmitted to progeny control gene expression to promote fertility. Germline-expressed small RNAs, including endogenous small interfering RNAs (endo-siRNAs) and Piwi-interacting RNAs (piRNAs), drive the repression of deleterious transcripts such as transposons, repetitive elements, and pseudogenes. Recent studies have highlighted an important role for small RNAs in transgenerational epigenetic inheritance via regulation of heritable chromatin marks; therefore, small RNAs are thought to convey an epigenetic memory of genomic self and nonself elements. Small RNA pathways are highly conserved in metazoans and have been best described for the model organism Caenorhabditis elegans. In this review, we describe the biogenesis, regulation, and function of C. elegans endo-siRNAs and piRNAs, along with recent insights into how these distinct pathways are integrated to collectively regulate germline gene expression, transgenerational epigenetic inheritance, and ultimately, animal fertility.


2021 ◽  
Vol 9 (2) ◽  
pp. 20
Author(s):  
Rwik Sen ◽  
Christopher Barnes

Epigenetic modifications regulate gene expression for development, immune response, disease, and other processes. A major role of epigenetics is to control the dynamics of chromatin structure, i.e., the condensed packaging of DNA around histone proteins in eukaryotic nuclei. Key epigenetic factors include enzymes for histone modifications and DNA methylation, non-coding RNAs, and prions. Epigenetic modifications are heritable but during embryonic development, most parental epigenetic marks are erased and reset. Interestingly, some epigenetic modifications, that may be resulting from immune response to stimuli, can escape remodeling and transmit to subsequent generations who are not exposed to those stimuli. This phenomenon is called transgenerational epigenetic inheritance if the epigenetic phenotype persists beyond the third generation in female germlines and second generation in male germlines. Although its primary function is likely immune response for survival, its role in the development and functioning of the immune system is not extensively explored, despite studies reporting transgenerational inheritance of stress-induced epigenetic modifications resulting in immune disorders. Hence, this review draws from studies on transgenerational epigenetic inheritance, immune system development and function, high-throughput epigenetics tools to study those phenomena, and relevant clinical trials, to focus on their significance and deeper understanding for future research, therapeutic developments, and various applications.


2019 ◽  
Vol 101 (5) ◽  
pp. 875-877
Author(s):  
Angela R Stermer ◽  
Shelby K Wilson ◽  
David Klein ◽  
Susan J Hall ◽  
Kim Boekelheide

Abstract Histone three lysine four dimethylation (H3k4me2) in sperm is conserved across species and is linked to transgenerational epigenetic inheritance. To test whether H3K4me2 is a target for transgenerational inheritance of toxicity, a daily gavage bolus exposure of trichloroethylene (TCE) (1000 mg/kg/day) was given to rats for 14 weeks, then epididymal sperm were isolated and native chromatin immunoprecipitation followed by next generation sequencing (ChIP-seq) of H3K4me2 was performed. Differential region analysis determined there were 2608 significantly differential H3K4me2 regions after TCE exposure, 477 were significantly increased and 2131 were significantly decreased. Z-score enrichment of differential regions determined there were significantly decreased H3k4me2 in the coding and regulatory regions of genes in the PKA signaling pathway. These changes account for TCE induced spermatozoal toxicity and show H3K4me2 is a target for paternal inheritance of toxicity.


Author(s):  
Eva Jablonka ◽  
Zohar Bronfman

Behavioral epigenetics is part of the thriving field of epigenetics, which describes the study of developmental processes that lead to persistent changes in the states of organisms, their components, and their lineages. Such developmental, context-sensitive changes are mediated by epigenetic mechanisms that establish and maintain the changes in patterns of gene expression and cellular structures that occur during ontogeny in both nondividing cells, such as most mature neurons, and dividing cells such as stem cells. When information is vertically transmitted to cells during cell division, or horizontally between cells through migrating reproducing molecules (like small RNAs), and when variations in the transmitted information are not determined by variations in DNA sequence (i.e., the same DNA sequence has more than one cell-heritable epigenetic state), epigenetic inheritance is said to occur. Behavioral epigenetics investigates the role of behavior in the shaping of developmental epigenetic states and the reciprocal role of epigenetic factors and mechanisms in the shaping of the behavior of human and nonhuman animals, at the short-, middle-, and long-term (ontogenetic, ecological, and evolutionary) time scales. The focus is on the molecular-epigenetic study of the interactions between environmental factors, such as ecological factors and habitual activities such as lifestyles and learning, with genetic variation and the neurobiological and physiological mechanisms that mediate between the regulation of gene expression and behavior. This range of epigenetic processes therefore includes, but is not limited to, studies involving epigenetic inheritance and the direct and indirect evolutionary effects of epigenetic developmental mechanisms. The neural-behavioral aspects that occur during ontogeny through the mediation of epigenetic mechanisms are central to behavioral epigenetics and are the main focus of neural epigenetics.


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