Meiotic progression in multinuclear mouse spermatocytes without the spindle pole clustering motor protein KIFC1 or cytokinesis forms single-cell late-stage spermatids

Mammalian spermatogenesis is a highly dynamic process involving male germ cell self-renewal and terminal differentiation into progenitor cells that produce testicular sperm in coordination with testicular somatic support cells. Multinuclear giant cells identified in mutant, toxin-exposed or genetically altered mice post-meiosis, reflect abnormal spermiogenesis. Here, analysis of fixed isolated testicular cells immunolabeled for microtubules, molecular motors, spindle binding proteins, and DNA from non-transgenic and GFP-CETN2-expressing CB6F1 or C57BL mice identify polynuclear primary spermatocytes within the normal testicular cell population. We hypothesize polynuclear primary spermatocytes arise from spermatogonia through aberrant cytokinesis or cell fusion of tethered spermatogonia. Polynuclear primary spermatocytes apparently progress in pre-prophase-I stages, completing first centriole duplication and homologous chromosome pairing/DNA cross-over events, forming multiple bipolar metaphase-I spindles of distinct phenotypes based on hypothesized spermatogonia derivation but without the microtubule clustering motor protein KIFC1. Remarkably, polynuclear spermatocytes are consistent with completing meiosis without undergoing first or second cytokinesis, seemingly generating polyploid spermatids post-meiosis. Polyploid spermatids perhaps undergo cytodifferentiation, forming sperm axonemes, acrosomes, centrosome nuclear binding, transient manchette microtubule assembly for nuclear shaping, associating with Sertoli cells and entering suspected spermiation. Collectively, these findings demonstrate remarkable testicular plasticity post-differentiation and the lax cell-cycle control of spermatogenesis, regardless of nuclear constituency.