The human zygote inherits its mitotic potential from the male gamete

Abstract

The control of centrosome and centriole duplication and formation of a single bipolar spindle during syngamy is different from that of somatic cells. If centrosomes from both gametes become functional, mosaicism could be induced following the formation of abnormal spindles. The centrosome used for development in most species is paternally inherited, with the exception of the mouse. Single and double centrioles within centrosomes in human zygotes have been described. Interpretation of data suggests that sperm centrioles are associated with further development. Here we provide evidence that the human sperm centrosome controls the first mitotic divisions after fertilization. Mosaicism and ploidy were determined in blastomeres derived from four groups of embryos: (i) dispermic zygotes, (ii) enucleated dispermic zygotes, (iii) monospermic zygotes in which the second polar body was retained (digynic), and (iv) enucleated monospermic digynic zygotes. Results prove that dispermic zygotes do not have bipolar spindles and become mosaic. This is determined by an extranuclear factor, since removal of a single pronucleus does not correct the abnormal division. Monospermic digynic embryos become triploid, indicating that the three pronuclei are organized in a single spindle and a single centrosome is active. Removal of one pronucleus from such zygotes causes the embryo to revert to a normal diploid state. These findings have consequences for the study of parthenogenesis, androgenesis and gynogenesis in the human.