Tudor domain containing 7 (Tdrd7) is essential for dynamic ribonucleoprotein (RNP) remodeling of chromatoid bodies during spermatogenesis

Takashi Tanaka, Mihoko Hosokawa, Vasily V. Vagin, Michael Reuter, Eri Hayashi, Ayako L. Mochizuki, Kouichi Kitamura, Hidenori Yamanaka, Gen Kondoh, Katsuya Okawa, Satomi Kuramochi-Miyagawa, Toru Nakano, Ravi Sachidanandam, Gregory J. Hannon, Ramesh S. Pillai, Norio Nakatsuji, Shinichiro Chuma

Research output: Contribution to journalArticlepeer-review

106 Scopus citations

Abstract

In the male germline in mammals, chromatoid bodies, a specialized assembly of cytoplasmic ribonucleoprotein (RNP), are structurally evident during meiosis and haploidgenesis, but their developmental origin and regulation remain elusive. The tudor domain containing proteins constitute a conserved class of chromatoid body components. We show that tudor domain containing 7 (Tdrd7), the deficiency of which causes male sterility and age-related cataract (as well as glaucoma), is essential for haploid spermatid development and defines, in concert with Tdrd6, key biogenesis processes of chromatoid bodies. Single and double knockouts of Tdrd7 and Tdrd6 demonstrated that these spermiogenic tudor genes orchestrate developmental programs for ordered remodeling of chromatoid bodies, including the initial establishment, subsequent RNP fusion with ubiquitous processing bodies/GW bodies and later structural maintenance. Tdrd7 suppresses LINE1 retrotransposons independently of piwi-interacting RNA (piRNA) biogenesis wherein Tdrd1 and Tdrd9 operate, indicating that distinct Tdrd pathways act against retrotransposons in the male germline. Tdrd6, in contrast, does not affect retrotransposons but functions at a later stage of spermiogenesis when chromatoid bodies exhibit aggresome-like properties. Our results delineate that chromatoid bodies assemble as an integrated compartment incorporating both germline and ubiquitous features as spermatogenesis proceeds and that the conserved tudor family genes act asmaster regulators of this unique RNP remodeling,which is genetically linked to the male germline integrity in mammals.

Original languageEnglish
Pages (from-to)10579-10584
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number26
DOIs
StatePublished - 28 Jun 2011

Keywords

  • Germ cells
  • Germinal granules
  • Nuage

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