The role of chromosome/kinetochore-driven microtubule generation in Drosophila spindle assembly.

In animal cells, proper spindle assembly requires generation of large numbers of microtubules (MTs) through three main pathways: MT nucleation by the centrosomes, nucleation near chromosomes/kinetochores and augmin-mediated nucleation from the walls of preexisting MTs. Here, we review the roles of these pathways in spindle assembly in different Drosophila tissues and cell types, with a focus on the chromosome/kinetochore-driven pathway. In female meiosis, there are no centrosomes, and the origin of spindle MTs is currently unclear. In embryos, larval brains and S2 cultured cells, the MTs generated by the mitotic chromatin are sufficient for the assembly of functional spindles, with different contributions of the augmin-dependent MTs. In contrast, in male meiotic cells the chromatin-driven MTs cannot form a functional spindle in the absence of centrosomal MTs, which can assemble a spindle even in the absence of chromosomes. Interestingly, in S2 cells chromatin-driven MTs are generated at kinetochores, as occurs in mammalian cells, while in embryos and larval brains they grow around chromosomes; in male meiotic cells MTs are generated both at kinetochores and around chromosomes. These results indicate that in Drosophila there is a remarkable flexibility in both the modes of chromatin-induced MT nucleation and the usage of MT generation pathways in spindle assembly. It remains to be determined whether a similar flexibility exists in other organisms, and to understand the molecular mechanisms that restrict MT nucleation at kinetochores in S2 cells. These studies will likely contribute to the elucidation of the mechanisms underlying kinetochore-induced MT formation in human cells.