Evidence map›Paper›PMID 32198406›Full record

ArticleNature communications2020

Reproductive tract extracellular vesicles are sufficient to transmit intergenerational stress and program neurodevelopment.

Jennifer C Chan, Christopher P Morgan, N Adrian Leu, Amol Shetty, Yasmine M Cisse, Bridget M Nugent, Kathleen E Morrison, Eldin Jašarević, Weiliang Huang, Nickole Kanyuch and 8 more

Open access · goldAbstract read
In one paragraph

Article in Nature communications, 2020. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 128 papers.

0numbers the graph read from it
0cells of the map it votes in
128citing papers in PubMed
11.6field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

128 citing papers in PubMed, 206 citations in OpenAlex.

  1. Article
  2. Article
  3. Review
  4. Article
  5. Review
  6. Article
  7. Article
  8. Review
  9. Article
  10. Article
  11. Article
  12. Article
  13. Review
  14. Article
  15. Review
  16. Review
  17. Environmental and Genetic Perturbations of the Sperm Epigenome.Advances in experimental medicine and biology · 2026
    Review
  18. Review
  19. Epididymosomes: Composition and Functions for Sperm Maturation.Advances in anatomy, embryology, and cell biology · 2026
    Review
  20. Review

68 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

18 authors at 2 institutions in 1 country.

Jennifer C ChanDepartment of Biomedical Sciences, School of Veterinary Medicine and Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Christopher P MorganDepartment of Pharmacology and Center for Epigenetic Research in Child Health and Brain Development, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
N Adrian LeuDepartment of Biomedical Sciences, School of Veterinary Medicine and Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Amol ShettyInstitute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
Yasmine M CisseDepartment of Pharmacology and Center for Epigenetic Research in Child Health and Brain Development, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
Bridget M NugentDepartment of Pharmacology and Center for Epigenetic Research in Child Health and Brain Development, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
Kathleen E MorrisonDepartment of Pharmacology and Center for Epigenetic Research in Child Health and Brain Development, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.ORCID http://orcid.org/0000-0002-3665-4757
Eldin JašarevićDepartment of Pharmacology and Center for Epigenetic Research in Child Health and Brain Development, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
Weiliang HuangDepartment of Pharmaceutical Science, University of Maryland School of Pharmacy, Baltimore, MD, 21201, USA.
Nickole KanyuchDepartment of Pharmacology and Center for Epigenetic Research in Child Health and Brain Development, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.ORCID http://orcid.org/0000-0003-4687-3803
Ali B RodgersDepartment of Biomedical Sciences, School of Veterinary Medicine and Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Natarajan V BhanuEpigenetics Institute, Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Dara S BergerDepartment of Obstetrics and Gynecology, Division of Reproductive Endocrinology and Infertility, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Benjamin A GarciaEpigenetics Institute, Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Seth AmentInstitute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.
Maureen KaneDepartment of Pharmaceutical Science, University of Maryland School of Pharmacy, Baltimore, MD, 21201, USA.
C Neill EppersonDepartment of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Tracy L BaleDepartment of Pharmacology and Center for Epigenetic Research in Child Health and Brain Development, University of Maryland School of Medicine, Baltimore, MD, 21201, USA. tbale@som.umaryland.edu.ORCID http://orcid.org/0000-0002-5017-5162
University of Maryland, Baltimore · USUniversity of Pennsylvania · US

Funding

Shared Resources Core 2: Quantitative Proteomics CoreP01CA196539 · NCI · ROCKEFELLER UNIVERSITY · PI GARCIA, BENJAMIN A · 2015 to 2024
$17.6M
Paternal stress epigenetic programming of offspring neurodevelopmentR37MH108286 · NIMH · UNIVERSITY OF PENNSYLVANIA · PI BALE, TRACY L · 2015 to 2024
$6.2M
Medical Scientist Training ProgramT32GM092237 · NIGMS · UNIVERSITY OF MARYLAND BALTIMORE · PI ROGHMANN, MARY-CLAIRE · 2010 to 2019
$3.0M
Placental epigenetic mechanisms contributing to sex-specific impacts of maternal stress on fetal developmentR01HD097093 · NICHD · UNIVERSITY OF MARYLAND BALTIMORE · PI BALE, TRACY L · 2019 to 2023
$2.4M
Female preconception stress programming of offspring neurodevelopmentR01ES028202 · NIEHS · UNIVERSITY OF MARYLAND BALTIMORE · PI BALE, TRACY L · 2017 to 2021
$2.2M
Maternal stress and the vaginal microbiome: impacts on brain developmentR33MH104184 · NIMH · UNIVERSITY OF PENNSYLVANIA · PI BALE, TRACY L · 2016 to 2018
$1.9M
Understanding the Role of Combinatorial Histone PTM PatternsR01GM110174 · NIGMS · UNIVERSITY OF PENNSYLVANIA · PI GARCIA, BENJAMIN A · 2014 to 2017
$1.3M
Immune and developmental actions of the maternal microbial metabolites on the hypothalamusK01DK121734 · NIDDK · UNIVERSITY OF MARYLAND BALTIMORE · PI JASAREVIC, ELDIN · 2020 to 2023
$555k
Maternal stress and the vaginal microbiome: impacts on brain developmentR21MH104184 · NIMH · UNIVERSITY OF PENNSYLVANIA · PI BALE, TRACY L · 2014 to 2015
$555k
NCI NIH HHS P01 CA196539NICHD NIH HHS R01 HD097093NIDDK NIH HHS K01 DK121734NIEHS NIH HHS R01 ES028202NIGMS NIH HHS R01 GM110174NIGMS NIH HHS T32 GM092237NIMH NIH HHS R21 MH104184NIMH NIH HHS R33 MH104184NIMH NIH HHS R37 MH108286
6 · The paper itself

Abstract

Extracellular vesicles (EVs) are a unique mode of intercellular communication capable of incredible specificity in transmitting signals involved in cellular function, including germ cell maturation. Spermatogenesis occurs in the testes, behind a protective barrier to ensure safeguarding of germline DNA from environmental insults. Following DNA compaction, further sperm maturation occurs in the epididymis. Here, we report reproductive tract EVs transmit information regarding stress in the paternal environment to sperm, potentially altering fetal development. Using intracytoplasmic sperm injection, we found that sperm incubated with EVs collected from stress-treated epididymal epithelial cells produced offspring with altered neurodevelopment and adult stress reactivity. Proteomic and transcriptomic assessment of these EVs showed dramatic changes in protein and miRNA content long after stress treatment had ended, supporting a lasting programmatic change in response to chronic stress. Thus, EVs as a normal process in sperm maturation, can also perform roles in intergenerational transmission of paternal environmental experience.

Indexed as

ProteomicsAdolescentAnimalsCell Culture TechniquesEpididymisEpigenesis, GeneticEpigenomicsExtracellular VesiclesFemaleGerm CellsHistonesHumansMaleMiceMice, Inbred C57BLMicroRNAsHistonesMicroRNAs

Identifiers

PMID32198406
PMCPMC7083921
OpenAlexW3011484207

What OpenQuestion holds

Textmetadata
LicenceCC BY
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.