The late chromatoid body component TSSK2 is involved in translational regulation in elongating spermatids in mice.

In brief: Temporally regulated translation is critical for late steps of spermatogenesis due to transcriptional silencing during chromatin condensation. This study shows that the function of the cytoplasmic granule, the late chromatoid body, is connected to translational regulation in condensing spermatids. Abstract: Spermatogenesis culminates in a dramatic morphological transformation, including a tight compaction of the chromatin and nuclear reshaping that largely silences transcription. Due to transcriptional silencing, the production of sperm-specific proteins needed for the morphological transformation requires active storage and translational regulation of mRNAs transcribed in earlier cell types. The germline-specific ribonucleoprotein (RNP) granule, the chromatoid body (CB), accumulates RNAs and has a role in RNA regulation in early haploid cells (round spermatids). In late haploid cells (elongating spermatids), the CB is transformed into the so-called late-CB, whose function in RNA regulation has remained elusive. Here we characterized the function of the late-CB by identifying proteins and RNAs interacting with the known late-CB marker, testis-specific serine/threonine-protein kinase 2 (TSSK2). We showed that TSSK2 and the late-CB associate with translation initiation factors and ribosomal proteins. Furthermore, we revealed an association of TSSK2 with a specific set of mRNAs that are enriched in polysome fractions in elongating spermatids, supporting the role of the late-CB in temporally regulated translation. These results link the function of the late-CB to RNA regulation during late spermatogenesis for the first time, providing important novel information about the RNA regulatory processes required for spermatogenesis and male fertility.