Somatic expression of piRNA and associated machinery in the mouse identifies short, tissue-specific piRNA

Bambarendage P.U. Perera, Zing Tsung Yeh Tsai, Mathia L. Colwell, Tamara R. Jones, Jaclyn M. Goodrich, Kai Wang, Maureen A. Sartor, Christopher Faulk, Dana C. Dolinoy

Research output: Contribution to journalArticlepeer-review

9 Scopus citations

Abstract

Piwi-interacting RNAs (piRNAs) are small non-coding RNAs that associate with PIWI proteins for transposon silencing via DNA methylation and are highly expressed and extensively studied in the germline. Mature germline piRNAs typically consist of 24–32 nucleotides, with a strong preference for a 5ʹ uridine signature, an adenosine signature at position 10, and a 2ʹ-O-methylation signature at the 3ʹ end. piRNA presence in somatic tissues, however, is not well characterized and requires further systematic evaluation. In the current study, we identified piRNAs and associated machinery from mouse somatic tissues representing the three germ layers. piRNA specificity was improved by combining small RNA size selection, sodium periodate treatment enrichment for piRNA over other small RNA, and small RNA next-generation sequencing. We identify PIWIL1, PIWIL2, and PIWIL4 expression in brain, liver, kidney, and heart. Of note, somatic piRNAs are shorter in length and tissue-specific, with increased occurrence of unique piRNAs in hippocampus and liver, compared to the germline. Hippocampus contains 5,494 piRNA-like peaks, the highest expression among all tested somatic tissues, followed by cortex (1,963), kidney (580), and liver (406). The study identifies 26 piRNA sequence species and 40 piRNA locations exclusive to all examined somatic tissues. Although piRNA expression has long been considered exclusive to the germline, our results support that piRNAs are expressed in several somatic tissues that may influence piRNA functions in the soma. Once confirmed, the PIWI/piRNA system may serve as a potential tool for future research in epigenome editing to improve human health by manipulating DNA methylation.

Original languageEnglish (US)
Pages (from-to)504-521
Number of pages18
JournalEpigenetics
Volume14
Issue number5
DOIs
StatePublished - May 4 2019

Bibliographical note

Funding Information:
This work was supported by the National Institute of Health (NIH) Director’s Transformative Award program and the National Institute of Environmental Health Sciences (NIEHS) [ES026877], with additional support from the Michigan Lifestage Environmental Exposures and Disease (M-LEEaD) NIEHS Core Center [P30 ES017885] and a NIEHS Pathways to Independence Award to CF [R00 ES022221];National Institute of Environmental Health Sciences [ES017885];National Institute of Environmental Health Sciences [ES026877];National Institute of Environmental Health Sciences [ES022221];

Funding Information:
This work was supported by the National Institute of Health (NIH) Director?s Transformative Award program and the National Institute of Environmental Health Sciences (NIEHS) [ES026877], with additional support from the Michigan Lifestage Environmental Exposures and Disease (M-LEEaD) NIEHS Core Center [P30 ES017885] and a NIEHS Pathways to Independence Award to CF [R00 ES022221];National Institute of Environmental Health Sciences [ES017885];National Institute of Environmental Health Sciences [ES026877];National Institute of Environmental Health Sciences [ES022221]; We thank the University of Michigan DNA Sequencing Core for their assistance with the library prep and sequencing the samples generated by the study, and the Zamore lab from the University of Massachusetts Medical School, for sharing the sodium periodate protocol with us.

Publisher Copyright:
© 2019, © 2019 Informa UK Limited, trading as Taylor & Francis Group.

Keywords

  • DNA methylation
  • Mouse
  • epigenome editing
  • piRNA
  • piwi
  • somatic

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