THE CENTROSOME AND ITS MODE OF INHERITANCE - THE REDUCTION OF THE CENTROSOME DURING GAMETOGENESIS AND ITS RESTORATION DURING FERTILIZATION

Neither the restoration of the centrosome during fertilization nor its reduction during gametogenesis is fully understood, but both are pivotal events in development. During each somatic cell cycle, the chromosomes, cytoplasm, and centrosomes duplicate in interphase, and all three split in two during each cell division. While it has long been recognized that both the sperm and the egg contribute equal haploid genomes during fertilization and that the vast majority of the cytoplasm is contributed by the egg, the relative contributions of the centrosome by each gamete are still in question. This article explores centrosome inheritance patterns and considers nine integral and secondarily derived activities of the centrosome. Boveri once hypothesized that ''The ripe egg possesses all of the elements necessary for development save an active division-center. The sperm, on the other hand, possesses such a center but lacks the protoplasmic substratum in which to operate. In this respect the egg and sperm are complementary structures; their union in syngamy thus restores to each the missing element necessary to further development.'' This article reviews the evidence gathered from 11 experimental strategies used to test this theory. While the majority of these approaches supports the hypothesis that the sperm introduces the centrosome at fertilization, the pattern did not reveal itself as universal, since parthenogenesis occurs in nature and can be induced artificially, since centrosome and centriole form de novo in extracts from unfertilized eggs and since the centrosome is derived from maternal sources during fertilization in some systems-notably, in mice. Models of the centrosome are proposed, along with speculative mechanisms which might lead to the cloaking of the reproducing element of the maternal centrosome during oogenesis and the retention of this structure by the paternal centrosome during spermatogenesis. Proteins essential for microtubule nucleation, like gamma-tubulin, are retained in the cytoplasm during oogenesis, but are largely lost during spermatogenesis. It is further postulated that the restoration of the zygotic centrosome at fertilization requires the attraction of maternal centrosomal components (in particular, gamma-tubulin and the 25S ''gamma-some'' particle) to the paternal reproducing element; this, along with post-translational modifications (including phosphorylation, disulfide reduction, and calcium ion binding), creates a functional zygote centrosome by blending both maternal and paternal constituents. Eggs capable of effecting parthenogenetic development, it is proposed, have a renaturable seed for centrosome reproduction and are therefore able to circumvent the requirement for paternal contribution. A model of centrosome behavior during gametogenesis and fertilization is presented: the sperm introduces the centrosome-reproducing element and a structure that attracts maternal proteins, including gamma-tubulin and the other proteins comprising the ''gamma-some.'' This concentration of gamma-tubulin initially nucleates the microtubules for the sperm aster and also attracts additional gamma-tubulin, resulting in the enlargement of the sperm aster. When the female pronucleus is contacted by the sperm astral microtubules, it moves toward the center of the sperm aster using dynein-like motors. The interaction between centrin in the sperm centrosome and the calcium released in the egg during activation is suggested to result in the excision of the sperm tail from the centrosome and sperm head, and also perhaps in the transformation of the basal body into the mature centrosome. Furthermore, the axonemal microtubules disassemble following sperm incorporation, and their disassembly requires microtubule dynamics. Fertilization is concluded when the parental genomes intermix; in humans, this occurs when chromosomes merge at the equator of the first mitotic spindle, which is anastral and often eccentric. The zygotic centrosome duplicates and splits immediately prior to the completion of the fertilization process. In essence, this model suggests that the zygote's centrosome is a blend of oocyte centrosomal proteins (including gamma-tubulin) attracted to the sperm's centrosome, which is capable of both binding gamma-tubulin and reproducing each cell cycle. (C) 1994 Academic Press, Inc.