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, Ali B. Rodgers, Natarajan V. Bhanu, Dara S. Berger, Benjamin A. Garcia, Seth Ament, Maureen Kane, C. Neill Epperson and Tracy L. Bale ()
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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

Nature Communications, 2020, vol. 11, issue 1, 1-13

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41467-020-15305-w

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