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

Author

Listed:
  • Jennifer C. Chan

    (University of Pennsylvania)

  • Christopher P. Morgan

    (University of Maryland School of Medicine)

  • N. Adrian Leu

    (University of Pennsylvania)

  • Amol Shetty

    (University of Maryland School of Medicine)

  • Yasmine M. Cisse

    (University of Maryland School of Medicine)

  • Bridget M. Nugent

    (University of Maryland School of Medicine)

  • Kathleen E. Morrison

    (University of Maryland School of Medicine)

  • Eldin Jašarević

    (University of Maryland School of Medicine)

  • Weiliang Huang

    (University of Maryland School of Pharmacy)

  • Nickole Kanyuch

    (University of Maryland School of Medicine)

  • Ali B. Rodgers

    (University of Pennsylvania)

  • Natarajan V. Bhanu

    (University of Pennsylvania)

  • Dara S. Berger

    (University of Pennsylvania)

  • Benjamin A. Garcia

    (University of Pennsylvania)

  • Seth Ament

    (University of Maryland School of Medicine)

  • Maureen Kane

    (University of Maryland School of Pharmacy)

  • C. Neill Epperson

    (University of Pennsylvania)

  • Tracy L. Bale

    (University of Maryland School of Medicine)

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.

Suggested Citation

  • 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 & Ali B. Rodge, 2020. "Reproductive tract extracellular vesicles are sufficient to transmit intergenerational stress and program neurodevelopment," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-15305-w
    DOI: 10.1038/s41467-020-15305-w
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    Cited by:

    1. Ariane Lismer & Sarah Kimmins, 2023. "Emerging evidence that the mammalian sperm epigenome serves as a template for embryo development," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Nickole Moon & Christopher P. Morgan & Ruth Marx-Rattner & Alyssa Jeng & Rachel L. Johnson & Ijeoma Chikezie & Carmen Mannella & Mary D. Sammel & C. Neill Epperson & Tracy L. Bale, 2024. "Stress increases sperm respiration and motility in mice and men," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    3. Yanwen Zhang & Li Ren & Xiaoxiao Sun & Zhilong Zhang & Jie Liu & Yining Xin & Jianmin Yu & Yimin Jia & Jinghao Sheng & Guo-fu Hu & Ruqian Zhao & Bin He, 2021. "Angiogenin mediates paternal inflammation-induced metabolic disorders in offspring through sperm tsRNAs," Nature Communications, Nature, vol. 12(1), pages 1-11, December.

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