The C. elegans zyg-1 Gene Encodes a Regulator of Centrosome Duplication with Distinct Maternal and Paternal Roles in the Embryo

Abstract

Centrosome duplication is a critical step in assembly of the bipolar mitotic spindle, but the molecular mechanisms regulating this process during the cell cycle and during animal development are poorly understood. Here, we report that the zyg-1 gene of Caenorhabditis elegans is an essential regulator of centrosome duplication. ZYG-1 is a protein kinase specifically required for daughter centriole formation that localizes transiently to centrosomes and acts at least one cell cycle prior to each spindle assembly event. In the embryo, ZYG-1 participates in a unique regulatory scheme whereby paternal ZYG-1 regulates duplication and bipolar spindle assembly during the first cell cycle, and maternal ZYG-1 regulates these processes thereafter. ZYG-1 is therefore a key molecular component of the centrosome/centriole duplication process.

γ-Tubulin-containing abnormal centrioles are induced by insufficient Plk4 in human HCT116 colorectal cancer cells

“…In C. elegans embryos, centriogenesis is triggered by a signal mediated by several key molecules, including ZYG-1 (O'Connell et al, 2001), which causes the targeting of SAS5 and SAS6 to a nascent centriole (Delattre et al, 2006;Pelletier et al, 2006). These molecules are required for formation and elongation of a central tube, a structural intermediate of the centriole, onto which nine sets of centriolar microtubules become organized in a SAS4-dependent manner (Pelletier et al, 2006).…”

The ZYG-1 kinase, a mitotic and meiotic regulator of centriole replication

“…What this means in genetic terms is that it is the genotype of the mother and not the zygote that determines the success of the early divisions. Only recently has an absolute requirement for paternal zyg-1 gene expression be demonstrated (O'Connell et al, 2001). This finding was somewhat unexpected as only a few paternal requirements for embryonic development had been demonstrated (Browning and Strome, 1996).…”

“…Recently, the zyg-1 gene of C. elegans has been identified as a regulator of centrosome replication (O'Connell et al, 2001). C. elegans is a free-living soil nematode with a hermaphroditic mode of reproduction.…”

“…The first zyg-1 allele was identified over 20 years ago as an embryonic lethal or zygote-defective mutation (Wood et al, 1980) but only recently has the basis for the embryonic lethality been determined (O'Connell et al, 2001). The offspring of mutant hermaphrodites fail to progress beyond the two-cell stage and exhibit defects in cell division during the first and/or second cell cycle.…”

“…In the past few years, several factors have been identified that regulate each of these steps. Among these factors is the ZYG-1 kinase of C. elegans, which functions during both mitotic and meiotic divisions (O'Connell et al, 2001).…”