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

Tanaka, T., Hosokawa, M., Vagin, V. V., Reuter, M., Hayashi, E., Mochizuki, A. L., Kitamura, K., Yamanaka, H., Kondoh, G., Okawa, K., Kuramochi-Miyagawa, S., Nakano, T., Sachidanandam, R., Hannon, G. J., Pillai, R. S., Nakatsuji, N., Chuma, S. (2011) Tudor domain containing 7 (Tdrd7) is essential for dynamic ribonucleoprotein (RNP) remodeling of chromatoid bodies during spermatogenesis. Proceedings of the National Academy of Sciences of the United States of America, 108 (26). pp. 10579-10584. ISSN 00278424 (ISSN)

[thumbnail of Paper]
Preview
PDF (Paper)
Hannon PNAS 2011.pdf - Published Version

Download (1MB) | Preview

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.

Item Type: Paper
Uncontrolled Keywords: Germ cells Germinal granules Nuage chromosome protein Piwi interacting RNA ribonucleoprotein tudor domain containing 1 protein tudor domain containing 6 protein tudor domain containing 7 protein tudor domain containing 9 protein unclassified drug aggresome animal experiment animal tissue article biogenesis cell maturation chromatid controlled study female gene inactivation glaucoma haploid spore male male sterility mouse nonhuman priority journal protein function protein processing protein structure retroposon senile cataract spermatid spermatogenesis Animals Chromatin Chromosomes, Artificial, Bacterial Mice Mice, Knockout Microscopy, Immunoelectron Ribonucleoproteins Mammalia
Subjects: bioinformatics > genomics and proteomics > genetics & nucleic acid processing
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types > RNP
CSHL Authors:
Communities: CSHL Cancer Center Program > Cancer Genetics
CSHL Cancer Center Shared Resources > Bioinformatics Service
CSHL Cancer Center Shared Resources > DNA Sequencing Service
CSHL Cancer Center Shared Resources > Microarray Service
CSHL Cancer Center Shared Resources > Microscopy Service
CSHL Post Doctoral Fellows
CSHL labs > Hannon lab
CSHL Cancer Center Shared Resources > Functional Genomics and Genetics Service
Depositing User: Matt Covey
Date: 2011
Date Deposited: 09 Jan 2013 16:17
Last Modified: 03 Jan 2018 17:27
PMCID: PMC3127926
Related URLs:
URI: https://repository.cshl.edu/id/eprint/26425

Actions (login required)

Administrator's edit/view item Administrator's edit/view item