Han Xue, Gomes José-Eduardo, Birmingham Cheryl L, Pintard Lionel, Sugimoto Asako, Mains Paul E
Genes and Development Research Group, Department of Biochemistry and Molecular Biology, University of Calgary, Alberta, Canada.
Genetics. 2009 Mar;181(3):933-43. doi: 10.1534/genetics.108.096016. Epub 2008 Dec 15.
MEI-1, the catalytic subunit of the Caenorhabditis elegans "katanin" microtubule-severing complex, is required for meiotic spindle formation. However, MEI-1 must be inactivated after the completion of meiosis to allow formation of the first mitotic spindle. Recent work demonstrated that post-meiotic MEI-1 undergoes ubiquitin-dependent degradation mediated by two independent pathways. Here we describe another level of MEI-1 regulation involving the protein phosphatase 4 (PP4) complex. The PP4 R1 regulatory subunit protein phosphatase four regulatory subunit 1 (ppfr-1) was identified in an RNA interference (RNAi) screen for suppressors of a mei-1(gf) allele that is refractory to post-meiotic degradation. RNAi to the PP4 catalytic subunit PPH-4.1 or to the alpha4 regulatory PPFR-4 also suppressed lethality of ectopic MEI-1. These results suggest that PP4(+) activates MEI-1, and therefore loss of PP4 decreases ectopic MEI-1(gf) activity. PPH-4.1 and MEI-1 co-immunoprecipitate with one another, indicating that the PP4 complex likely regulates MEI-1 activity directly rather than through an intermediate. The ppfr-1 mutant has subtle meiotic defects indicating that PPFR-1 also regulates MEI-1 during meiosis. MBK-2 is the only kinase known to phosphorylate MEI-1 and triggers post-meiotic MEI-1 degradation. However, genetic interactions between PP4 and mbk-2 were not consistent with an antagonistic relationship between the phosphatase and kinase. Additionally, reducing PP4 in mei-1(gf) did not change the level or localization of post-meiotic MEI-1. Thus, by making use of a genetic background where MEI-1 is ectopically expressed, we have uncovered a third mechanism of MEI-1 regulation, one based on phosphorylation but independent of degradation. The redundant regulatory pathways likely contribute in different ways to the rapid and precise post-meiotic inactivation of MEI-1 microtubule-severing activity.
MEI-1是秀丽隐杆线虫“katanin”微管切断复合物的催化亚基,是减数分裂纺锤体形成所必需的。然而,减数分裂完成后MEI-1必须失活,以便形成第一个有丝分裂纺锤体。最近的研究表明,减数分裂后的MEI-1通过两条独立途径进行泛素依赖性降解。在这里,我们描述了MEI-1调控的另一个层面,涉及蛋白磷酸酶4(PP4)复合物。在对减数分裂后降解具有抗性的mei-1(gf)等位基因的抑制子进行的RNA干扰(RNAi)筛选中,鉴定出了PP4 R1调节亚基蛋白磷酸酶4调节亚基1(ppfr-1)。对PP4催化亚基PPH-4.1或α4调节亚基PPFR-4进行RNAi也可抑制异位MEI-1的致死性。这些结果表明PP4(+)激活MEI-1,因此PP4的缺失会降低异位MEI-1(gf)的活性。PPH-4.1和MEI-1相互共免疫沉淀,表明PP4复合物可能直接调节MEI-1的活性,而不是通过中间体。ppfr-1突变体有轻微的减数分裂缺陷,表明PPFR-1在减数分裂期间也调节MEI-1。MBK-2是已知的唯一能磷酸化MEI-1并触发减数分裂后MEI-1降解的激酶。然而,PP4和mbk-2之间的遗传相互作用与磷酸酶和激酶之间的拮抗关系不一致。此外,在mei-1(gf)中降低PP4水平并不会改变减数分裂后MEI-1的水平或定位。因此,通过利用MEI-1异位表达的遗传背景,我们发现了MEI-1调控的第三种机制,一种基于磷酸化但独立于降解的机制。这些冗余的调控途径可能以不同方式对MEI-1微管切断活性的快速和精确的减数分裂后失活做出贡献。