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Angiogenin mediates paternal inflammation-induced metabolic disorders in offspring through sperm tsRNAs

Author

Listed:
  • Yanwen Zhang

    (Nanjing Agricultural University)

  • Li Ren

    (Nanjing Agricultural University)

  • Xiaoxiao Sun

    (Nanjing Agricultural University)

  • Zhilong Zhang

    (Nanjing Agricultural University)

  • Jie Liu

    (Nanjing Agricultural University)

  • Yining Xin

    (Nanjing Agricultural University)

  • Jianmin Yu

    (Zhejiang University School of Medicine)

  • Yimin Jia

    (Nanjing Agricultural University
    Nanjing Agricultural University)

  • Jinghao Sheng

    (Zhejiang University School of Medicine)

  • Guo-fu Hu

    (Tufts Medical Center)

  • Ruqian Zhao

    (Nanjing Agricultural University
    Nanjing Agricultural University)

  • Bin He

    (Nanjing Agricultural University
    Nanjing Agricultural University)

Abstract

Paternal environmental inputs can influence various phenotypes in offspring, presenting tremendous implications for basic biology and public health and policy. However, which signals function as a nexus to transmit paternal environmental inputs to offspring remains unclear. Here we show that offspring of fathers with inflammation exhibit metabolic disorders including glucose intolerance and obesity. Deletion of a mouse tRNA RNase, Angiogenin (Ang), abolished paternal inflammation-induced metabolic disorders in offspring. Additionally, Ang deletion prevented the inflammation-induced alteration of 5′-tRNA-derived small RNAs (5′-tsRNAs) expression profile in sperm, which might be essential in composing a sperm RNA ‘coding signature’ that is needed for paternal epigenetic memory. Microinjection of sperm 30–40 nt RNA fractions (predominantly 5′-tsRNAs) from inflammatory Ang+/+ males but not Ang–/– males resulted in metabolic disorders in the resultant offspring. Moreover, zygotic injection with synthetic 5′-tsRNAs which increased in inflammatory mouse sperm and decreased by Ang deletion partially resembled paternal inflammation-induced metabolic disorders in offspring. Together, our findings demonstrate that Ang-mediated biogenesis of 5′-tsRNAs in sperm contributes to paternal inflammation-induced metabolic disorders in offspring.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26909-1
    DOI: 10.1038/s41467-021-26909-1
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    References listed on IDEAS

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    1. 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.
    2. Dora L. Costa & Noelle Yetter & Heather DeSomer, 2018. "Intergenerational transmission of paternal trauma among US Civil War ex-POWs," Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, vol. 115(44), pages 11215-11220, October.
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