Developmental origins of transgenerational sperm histone retention following ancestral exposures

Maamar, Millissia Ben; Beck, Daniel; Nilsson, Eric; McCarrey, John R.; Skinner, Michael K.

doi:10.1016/j.ydbio.2020.06.008

Cited by 20 publications

(20 citation statements)

References 86 publications

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“…It has been shown that sperm DNA methylation is altered by various environmental exposures in mice, and it contributes to transgenerational epigenetic inheritance (Radford et al, 2014 ). Recent work points toward the possible mechanism for transmitting paternal environmental exposures to the next generation, via sperm DNA methylation, ncRNAs and histone retention (Ben Maamar et al, 2020 ). Additionally, age-related methylation changes are well-documented in human sperm; more recent studies shed light on this in bulls as well (Lambert et al, 2018 ; Takeda et al, 2019 ; Khezri et al, 2020 ; Wu et al, 2020a ).…”

Section: Transgenerational Epigenetic Inheritance In Livestock Speciementioning

confidence: 99%

The Epigenetics of Gametes and Early Embryos and Potential Long-Range Consequences in Livestock Species—Filling in the Picture With Epigenomic Analyses

2021

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The epigenome is dynamic and forged by epigenetic mechanisms, such as DNA methylation, histone modifications, chromatin remodeling, and non-coding RNA species. Increasing lines of evidence support the concept that certain acquired traits are derived from environmental exposure during early embryonic and fetal development, i.e., fetal programming, and can even be “memorized” in the germline as epigenetic information and transmitted to future generations. Advances in technology are now driving the global profiling and precise editing of germline and embryonic epigenomes, thereby improving our understanding of epigenetic regulation and inheritance. These achievements open new avenues for the development of technologies or potential management interventions to counteract adverse conditions or improve performance in livestock species. In this article, we review the epigenetic analyses (DNA methylation, histone modification, chromatin remodeling, and non-coding RNAs) of germ cells and embryos in mammalian livestock species (cattle, sheep, goats, and pigs) and the epigenetic determinants of gamete and embryo viability. We also discuss the effects of parental environmental exposures on the epigenetics of gametes and the early embryo, and evidence for transgenerational inheritance in livestock.

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Section: Transgenerational Epigenetic Inheritance In Livestock Speciementioning

confidence: 99%

The Epigenetics of Gametes and Early Embryos and Potential Long-Range Consequences in Livestock Species—Filling in the Picture With Epigenomic Analyses

2021

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“…Therefore, it becomes essential for the animal to discriminate between pathogenic versus nonpathogenic chemical environments to display appropriate behaviors. Specific olfactory neurons sense soluble and volatile chemicals from the biotic environment (10,11) to mediate attraction or aversion to pathogenic and commensal bacteria (9,(12)(13)(14). Interestingly, a number of potentially pathogenic bacteria are attractive at first since they also produce attractive odorants (15) or contain metabolites of high nutritional value such as vitamin B12 (16).…”

Section: Sensing the Biotic Environment And The Creation Of A Chemical Memorymentioning

confidence: 99%

“…Chemical information about the intestinal luminal environment is transmitted to the CNS through the vagus nerve in mammals ( 29 ), and through the recurrent nerve in insects, like Drosophila ( 30 ). In C. elegans , sensory neurons detect microbial metabolites such as bacterial autoinducers [homoserine lactones ( 12 ), (S)-3-hydroxytridecan-4-one ( 15 ), and other virulence factors like phenazine and pyochelin ( 19 ). to coordinate behaviors like avoidance ( 12 , 13 , 19 ) and attraction ( 15 ).…”

Section: Sensing the Biotic Environment And The Creation Of A Chemical Memorymentioning

confidence: 99%

The Heritability of Behaviors Associated With the Host Gut Microbiota

2021

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What defines whether the interaction between environment and organism creates a genetic memory able to be transferred to subsequent generations? Bacteria and the products of their metabolism are the most ubiquitous biotic environments to which every living organism is exposed. Both microbiota and host establish a framework where environmental and genetic factors are integrated to produce adaptive life traits, some of which can be inherited. Thus, the interplay between host and microbe is a powerful model to study how phenotypic plasticity is inherited. Communication between host and microbe can occur through diverse molecules such as small RNAs (sRNAs) and the RNA interference machinery, which have emerged as mediators and carriers of heritable environmentally induced responses. Notwithstanding, it is still unclear how the organism integrates sRNA signaling between different tissues to orchestrate a systemic bacterially induced response that can be inherited. Here we discuss current evidence of heritability produced by the intestinal microbiota from several species. Neurons and gut are the sensing systems involved in transmitting changes through transcriptional and post-transcriptional modifications to the gonads. Germ cells express inflammatory receptors, and their development and function are regulated by host and bacterial metabolites and sRNAs thus suggesting that the dynamic interplay between host and microbe underlies the host’s capacity to transmit heritable behaviors. We discuss how the host detects changes in the microbiota that can modulate germ cells genomic functions. We also explore the nature of the interactions that leave permanent or long-term memory in the host and propose mechanisms by which the microbiota can regulate the development and epigenetic reprogramming of germ cells, thus influencing the inheritance of the host. We highlight the vast contribution of the bacterivore nematode C. elegans and its commensal and pathogenic bacteria to the understanding on how behavioral adaptations can be inter and transgenerational inherited.

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“…Chromatin Immunoprecipitation (ChIP). As previously described in [79], Histone chromatin immunoprecipitation with genomic DNA was performed with a procedure previously described [35]. Individual rat sperm collections were generated, and the sperm counts were determined for each individual.…”

Section: Sperm Epigenetic Analysismentioning

confidence: 99%

Epigenome-wide association study for atrazine induced transgenerational DNA methylation and histone retention sperm epigenetic biomarkers for disease

et al. 2020

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Atrazine is a common agricultural herbicide previously shown to promote epigenetic transgenerational inheritance of disease to subsequent generations. The current study was designed as an epigenome-wide association study (EWAS) to identify transgenerational sperm disease associated differential DNA methylation regions (DMRs) and differential histone retention regions (DHRs). Gestating female F0 generation rats were transiently exposed to atrazine during the period of embryonic gonadal sex determination, and then subsequent F1, F2, and F3 generations obtained in the absence of any continued exposure. The transgenerational F3 generation males were assessed for disease and sperm collected for epigenetic analysis. Pathology was observed in pubertal onset and for testis disease, prostate disease, kidney disease, lean pathology, and multiple disease. For these pathologies, sufficient numbers of individual males with only a single specific disease were identified. The sperm DNA and chromatin were isolated from adult one-year animals with the specific diseases and analyzed for DMRs with methylated DNA immunoprecipitation (MeDIP) sequencing and DHRs with histone chromatin immunoprecipitation (ChIP) sequencing. Transgenerational F3 generation males with or without disease were compared to identify the disease specific epimutation biomarkers. All pathologies were found to have disease specific DMRs and DHRs which were found to predominantly be distinct for each disease. No common DMRs or DHRs were found among all the pathologies. Epimutation gene associations were identified and found to correlate to previously known disease linked genes. This is one of the first observations of potential sperm disease biomarkers for histone retention sites. Although further studies with expanded animal numbers are required, the current study provides evidence the EWAS analysis is effective for the identification of potential pathology epimutation biomarkers for disease susceptibility.

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Developmental origins of transgenerational sperm histone retention following ancestral exposures

Cited by 20 publications

References 86 publications

The Epigenetics of Gametes and Early Embryos and Potential Long-Range Consequences in Livestock Species—Filling in the Picture With Epigenomic Analyses

The Epigenetics of Gametes and Early Embryos and Potential Long-Range Consequences in Livestock Species—Filling in the Picture With Epigenomic Analyses

The Heritability of Behaviors Associated With the Host Gut Microbiota

Epigenome-wide association study for atrazine induced transgenerational DNA methylation and histone retention sperm epigenetic biomarkers for disease

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