Conserved piRNA Expression from a Distinct Set of piRNA Cluster Loci in Eutherian Mammals

Gung Wei Chirn, Reazur Rahman, Yuliya A. Sytnikova, Jessica A. Matts, Mei Zeng, Daniel Gerlach, Michael Yu, Bonnie Berger, Mayumi Naramura, Benjamin T. Kile, Nelson C. Lau

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

The Piwi pathway is deeply conserved amongst animals because one of its essential functions is to repress transposons. However, many Piwi-interacting RNAs (piRNAs) do not base-pair to transposons and remain mysterious in their targeting function. The sheer number of piRNA cluster (piC) loci in animal genomes and infrequent piRNA sequence conservation also present challenges in determining which piC loci are most important for development. To address this question, we determined the piRNA expression patterns of piC loci across a wide phylogenetic spectrum of animals, and reveal that most genic and intergenic piC loci evolve rapidly in their capacity to generate piRNAs, regardless of known transposon silencing function. Surprisingly, we also uncovered a distinct set of piC loci with piRNA expression conserved deeply in Eutherian mammals. We name these loci Eutherian-Conserved piRNA cluster (ECpiC) loci. Supporting the hypothesis that conservation of piRNA expression across ~100 million years of Eutherian evolution implies function, we determined that one ECpiC locus generates abundant piRNAs antisense to the STOX1 transcript, a gene clinically associated with preeclampsia. Furthermore, we confirmed reduced piRNAs in existing mouse mutations at ECpiC-Asb1 and -Cbl, which also display spermatogenic defects. The Asb1 mutant testes with strongly reduced Asb1 piRNAs also exhibit up-regulated gene expression profiles. These data indicate ECpiC loci may be specially adapted to support Eutherian reproduction.

Original languageEnglish (US)
Article numbere1005652
JournalPLoS genetics
Volume11
Issue number11
DOIs
StatePublished - Nov 2015

Fingerprint

Small Interfering RNA
RNA
Mammals
mammal
mammals
loci
small interfering RNA
animal
transposons
targeting
gene expression
defect
mutation
genome
pre-eclampsia
animals
phylogenetics
gene
testes
mutants

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Chirn, G. W., Rahman, R., Sytnikova, Y. A., Matts, J. A., Zeng, M., Gerlach, D., ... Lau, N. C. (2015). Conserved piRNA Expression from a Distinct Set of piRNA Cluster Loci in Eutherian Mammals. PLoS genetics, 11(11), [e1005652]. https://doi.org/10.1371/journal.pgen.1005652

Conserved piRNA Expression from a Distinct Set of piRNA Cluster Loci in Eutherian Mammals. / Chirn, Gung Wei; Rahman, Reazur; Sytnikova, Yuliya A.; Matts, Jessica A.; Zeng, Mei; Gerlach, Daniel; Yu, Michael; Berger, Bonnie; Naramura, Mayumi; Kile, Benjamin T.; Lau, Nelson C.

In: PLoS genetics, Vol. 11, No. 11, e1005652, 11.2015.

Research output: Contribution to journalArticle

Chirn, GW, Rahman, R, Sytnikova, YA, Matts, JA, Zeng, M, Gerlach, D, Yu, M, Berger, B, Naramura, M, Kile, BT & Lau, NC 2015, 'Conserved piRNA Expression from a Distinct Set of piRNA Cluster Loci in Eutherian Mammals', PLoS genetics, vol. 11, no. 11, e1005652. https://doi.org/10.1371/journal.pgen.1005652
Chirn GW, Rahman R, Sytnikova YA, Matts JA, Zeng M, Gerlach D et al. Conserved piRNA Expression from a Distinct Set of piRNA Cluster Loci in Eutherian Mammals. PLoS genetics. 2015 Nov;11(11). e1005652. https://doi.org/10.1371/journal.pgen.1005652
Chirn, Gung Wei ; Rahman, Reazur ; Sytnikova, Yuliya A. ; Matts, Jessica A. ; Zeng, Mei ; Gerlach, Daniel ; Yu, Michael ; Berger, Bonnie ; Naramura, Mayumi ; Kile, Benjamin T. ; Lau, Nelson C. / Conserved piRNA Expression from a Distinct Set of piRNA Cluster Loci in Eutherian Mammals. In: PLoS genetics. 2015 ; Vol. 11, No. 11.
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