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

Yanwen Zhang, Li Ren, Xiaoxiao Sun, Zhilong Zhang, Jie Liu, Yining Xin, Jianmin Yu, Yimin Jia, Jinghao Sheng, Guo-fu Hu, Ruqian Zhao and Bin He ()
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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
Jinghao Sheng: Zhejiang University School of Medicine
Guo-fu Hu: Tufts Medical Center
Ruqian Zhao: Nanjing Agricultural University
Bin He: Nanjing Agricultural University

Nature Communications, 2021, vol. 12, issue 1, 1-11

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-26909-1

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