MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis

Katsuhiko Hayashi, Susana M. Chuva de Sousa Lopes, Masahiro Kaneda, Fuchou Tang, Petra Hajkova, Kaiqin Lao, Donai O'Carroll, Partha P. Das, Alexander Tarakhovsky, Eric A. Miska, M. Azim Surani

Research output: Contribution to journalArticle

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Abstract

Background: MicroRNAs (miRNAs) are critical regulators of transcriptional and post-transcriptional gene silencing, which are involved in multiple develpment processes in many organisms. Apart from miRNAs, mouse germ cells express another type of small RNA, piwi-interacting RNAs (piRNAs). Although it has been clear that piRNAs play a role in repression of retrotransposons during spermatogenesis, the function of miRNA in mouse germ cells has been unclear. Methodology/Principle Findings: In this study, we first revealed the expression pattern of miRNAs by using a real-time PCR-based 220 plex miRNA expression profiling method. During development of germ cells, miR-17-92 cluster, which is thought to promote cell cycling, and the ES cell-specific cluster encoding miR-290 to -295 (miR-290-295 cluster) were highly expressed in primordial germ cells (PGCs) and spermatogonia. A set of miRNAs was developmentally regulated. We next analysed function of miRNA biogenesis in germ cell development by using conditional Dicer-knockout mice in which Dicer gene was deleted specifically in the germ cells. Dicer-deleted PGCs and spermatogonia exhibited poor proliferation. Retrotransposon activity was unexpectedly suppressed in Dicer-deleted PGCs, but not affected in the spermatogonia. In Dicer-deleted testis, spermatogenesis was retarded at an early stage when proliferation and/or early differentiation. Additionally, we analysed spermatogenesis in conditional Argonaute2-deficient mice. In contrast to Dicer-deficient testis, spermatogenesis in Argonaute2-deficient testis was indistinguishable from that in wild type. Conclusion/Significance: These results illustrate that miRNAs are important for the proliferation of PGCs and spermatogonia, but dispensable for the repression of retrotransposons in developing germ cells. Consistently, miRNAs promoting cell cycling are highly expressed in PGCs and spermatogonia. Furthermore, based on normal spermatogenesis in Argonaute2-deficient testis, the critical function of Dicer in spermatogenesis is independent of Argonaute2.

Original languageEnglish
Article numbere1738
JournalPloS one
Volume3
Issue number3
DOIs
Publication statusPublished - Mar 5 2008

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Spermatogenesis
spermatogenesis
MicroRNAs
microRNA
Germ Cells
germ cells
Cells
Spermatogonia
mice
spermatogonia
Retroelements
Testis
testes
retrotransposons
Small Interfering RNA
small interfering RNA
Genes
biogenesis
RNA
cells

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

Cite this

Hayashi, K., Chuva de Sousa Lopes, S. M., Kaneda, M., Tang, F., Hajkova, P., Lao, K., ... Surani, M. A. (2008). MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PloS one, 3(3), [e1738]. https://doi.org/10.1371/journal.pone.0001738

MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. / Hayashi, Katsuhiko; Chuva de Sousa Lopes, Susana M.; Kaneda, Masahiro; Tang, Fuchou; Hajkova, Petra; Lao, Kaiqin; O'Carroll, Donai; Das, Partha P.; Tarakhovsky, Alexander; Miska, Eric A.; Surani, M. Azim.

In: PloS one, Vol. 3, No. 3, e1738, 05.03.2008.

Research output: Contribution to journalArticle

Hayashi, K, Chuva de Sousa Lopes, SM, Kaneda, M, Tang, F, Hajkova, P, Lao, K, O'Carroll, D, Das, PP, Tarakhovsky, A, Miska, EA & Surani, MA 2008, 'MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis', PloS one, vol. 3, no. 3, e1738. https://doi.org/10.1371/journal.pone.0001738
Hayashi, Katsuhiko ; Chuva de Sousa Lopes, Susana M. ; Kaneda, Masahiro ; Tang, Fuchou ; Hajkova, Petra ; Lao, Kaiqin ; O'Carroll, Donai ; Das, Partha P. ; Tarakhovsky, Alexander ; Miska, Eric A. ; Surani, M. Azim. / MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. In: PloS one. 2008 ; Vol. 3, No. 3.
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