Crystal Structure of Silkworm PIWI-Clade Argonaute Siwi Bound to piRNA

Naoki Matsumoto, Hiroshi Nishimasu, Kazuhiro Sakakibara, Kazumichi M. Nishida, Takamasa Hirano, Ryuichiro Ishitani, Haruhiko Siomi, Mikiko C. Siomi, Osamu Nureki

Research output: Contribution to journalArticle

40 Citations (Scopus)

Abstract

PIWI-clade Argonaute proteins associate with PIWI-interacting RNAs (piRNAs) and silence transposable elements in animal gonads. Here, we report the crystal structure of a silkworm PIWI-clade Argonaute, Siwi, bound to the endogenous piRNA, at 2.4 Å resolution. Siwi adopts a bilobed architecture consisting of N-PAZ and MID-PIWI lobes, in which the 5′ and 3′ ends of the bound piRNA are anchored by the MID-PIWI and PAZ domains, respectively. A structural comparison of Siwi with AGO-clade Argonautes reveals notable differences in their nucleic-acid-binding channels, likely reflecting the distinct lengths of their guide RNAs and their mechanistic differences in guide RNA loading and cleavage product release. In addition, the structure reveals that Siwi and prokaryotic, but not eukaryotic, AGO-clade Argonautes share unexpected similarities, such as metal-dependent 5′-phosphate recognition and a potential structural transition during the catalytic-tetrad formation. Overall, this study provides a critical starting point toward a mechanistic understanding of piRNA-mediated transposon silencing.

Original languageEnglish
Pages (from-to)484-497.e9
JournalCell
Volume167
Issue number2
DOIs
Publication statusPublished - 2016 Oct 6

Fingerprint

Bombyx
Guide RNA
Small Interfering RNA
Crystal structure
Argonaute Proteins
RNA Cleavage
DNA Transposable Elements
Gonads
Nucleic Acids
Animals
Metals
Phosphates
RNA

Keywords

  • 1U bias
  • Argonaute
  • piRNA
  • PIWI
  • RNA silencing
  • Siwi
  • small RNA
  • x-ray crystallography

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Matsumoto, N., Nishimasu, H., Sakakibara, K., Nishida, K. M., Hirano, T., Ishitani, R., ... Nureki, O. (2016). Crystal Structure of Silkworm PIWI-Clade Argonaute Siwi Bound to piRNA. Cell, 167(2), 484-497.e9. https://doi.org/10.1016/j.cell.2016.09.002

Crystal Structure of Silkworm PIWI-Clade Argonaute Siwi Bound to piRNA. / Matsumoto, Naoki; Nishimasu, Hiroshi; Sakakibara, Kazuhiro; Nishida, Kazumichi M.; Hirano, Takamasa; Ishitani, Ryuichiro; Siomi, Haruhiko; Siomi, Mikiko C.; Nureki, Osamu.

In: Cell, Vol. 167, No. 2, 06.10.2016, p. 484-497.e9.

Research output: Contribution to journalArticle

Matsumoto, N, Nishimasu, H, Sakakibara, K, Nishida, KM, Hirano, T, Ishitani, R, Siomi, H, Siomi, MC & Nureki, O 2016, 'Crystal Structure of Silkworm PIWI-Clade Argonaute Siwi Bound to piRNA', Cell, vol. 167, no. 2, pp. 484-497.e9. https://doi.org/10.1016/j.cell.2016.09.002
Matsumoto N, Nishimasu H, Sakakibara K, Nishida KM, Hirano T, Ishitani R et al. Crystal Structure of Silkworm PIWI-Clade Argonaute Siwi Bound to piRNA. Cell. 2016 Oct 6;167(2):484-497.e9. https://doi.org/10.1016/j.cell.2016.09.002
Matsumoto, Naoki ; Nishimasu, Hiroshi ; Sakakibara, Kazuhiro ; Nishida, Kazumichi M. ; Hirano, Takamasa ; Ishitani, Ryuichiro ; Siomi, Haruhiko ; Siomi, Mikiko C. ; Nureki, Osamu. / Crystal Structure of Silkworm PIWI-Clade Argonaute Siwi Bound to piRNA. In: Cell. 2016 ; Vol. 167, No. 2. pp. 484-497.e9.
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