Transgenerational epigenetic reprogramming of early embryos: a mechanistic model

Abstract The notion that epigenetic information can be transmitted across generations is supported by mounting waves of data, but the underlying mechanisms remain elusive. Here, a model is proposed which combines different lines of experimental evidence. First, it has been shown that somatic tissues...

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Published inEnvironmental epigenetics Vol. 6; no. 1; p. dvaa009
Main Author Spadafora, Corrado
Format Journal Article
LanguageEnglish
Published Oxford University Press 01.01.2020
Subjects
Review
extracellular vesicles
sperm RNA
chromatin remodeling
Waddington
early embryos
sperm cells
epigenetic inheritance
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Abstract Abstract The notion that epigenetic information can be transmitted across generations is supported by mounting waves of data, but the underlying mechanisms remain elusive. Here, a model is proposed which combines different lines of experimental evidence. First, it has been shown that somatic tissues exposed to stressing stimuli release circulating RNA-containing extracellular vesicles; second, epididymal spermatozoa can take up, internalize and deliver the RNA-containing extracellular vesicles to oocytes at fertilization; third, early embryos can process RNA-based information. These elements constitute the building blocks upon which the model is built. The model proposes that a continuous stream of epigenetic information flows from parental somatic tissues to the developing embryos. The flow can cross the Weismann barrier, is mediated by circulating vesicles and epididymal spermatozoa, and has the potential to generate epigenetic traits that are then stably acquired in the offspring. In a broader perspective, it emerges that a natural ‘assembly line’ operates continuously, aiming at passing the parental epigenetic blueprint in growing embryos.
AbstractList Abstract The notion that epigenetic information can be transmitted across generations is supported by mounting waves of data, but the underlying mechanisms remain elusive. Here, a model is proposed which combines different lines of experimental evidence. First, it has been shown that somatic tissues exposed to stressing stimuli release circulating RNA-containing extracellular vesicles; second, epididymal spermatozoa can take up, internalize and deliver the RNA-containing extracellular vesicles to oocytes at fertilization; third, early embryos can process RNA-based information. These elements constitute the building blocks upon which the model is built. The model proposes that a continuous stream of epigenetic information flows from parental somatic tissues to the developing embryos. The flow can cross the Weismann barrier, is mediated by circulating vesicles and epididymal spermatozoa, and has the potential to generate epigenetic traits that are then stably acquired in the offspring. In a broader perspective, it emerges that a natural ‘assembly line’ operates continuously, aiming at passing the parental epigenetic blueprint in growing embryos.
The notion that epigenetic information can be transmitted across generations is supported by mounting waves of data, but the underlying mechanisms remain elusive. Here, a model is proposed which combines different lines of experimental evidence. First, it has been shown that somatic tissues exposed to stressing stimuli release circulating RNA-containing extracellular vesicles; second, epididymal spermatozoa can take up, internalize and deliver the RNA-containing extracellular vesicles to oocytes at fertilization; third, early embryos can process RNA-based information. These elements constitute the building blocks upon which the model is built. The model proposes that a continuous stream of epigenetic information flows from parental somatic tissues to the developing embryos. The flow can cross the Weismann barrier, is mediated by circulating vesicles and epididymal spermatozoa, and has the potential to generate epigenetic traits that are then stably acquired in the offspring. In a broader perspective, it emerges that a natural ‘assembly line’ operates continuously, aiming at passing the parental epigenetic blueprint in growing embryos.
Author Spadafora, Corrado
AuthorAffiliation Institute of Translational Pharmacology, National Research Council (CNR) , 100 Via del Fosso del Cavaliere, 00133 Rome, Italy
AuthorAffiliation_xml – name: Institute of Translational Pharmacology, National Research Council (CNR) , 100 Via del Fosso del Cavaliere, 00133 Rome, Italy
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  givenname: Corrado
  orcidid: 0000-0002-5743-3224
  surname: Spadafora
  fullname: Spadafora, Corrado
  email: corrado.spadafora@gmail.com
  organization: Institute of Translational Pharmacology, National Research Council (CNR), 100 Via del Fosso del Cavaliere, 00133 Rome, Italy
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Issue 1
Keywords extracellular vesicles
sperm RNA
chromatin remodeling
Waddington
early embryos
sperm cells
epigenetic inheritance
Language English
License This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
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Snippet Abstract The notion that epigenetic information can be transmitted across generations is supported by mounting waves of data, but the underlying mechanisms...
The notion that epigenetic information can be transmitted across generations is supported by mounting waves of data, but the underlying mechanisms remain...
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SubjectTerms Review
Title Transgenerational epigenetic reprogramming of early embryos: a mechanistic model
URI https://search.proquest.com/docview/2427301531
https://pubmed.ncbi.nlm.nih.gov/PMC7368376
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