Background/Significance:
The Eyes Absent gene family (EYA1-4) are a unique group of tyrosine phosphatases that are often mis-regulated in cancer. EYA1 and EYA4 are highly expressed in several tumours of neurological origin that are common in children, including glioma, MPNST, and high-risk neuroblastoma. Mounting evidence suggests that the EYAs play an oncogenic role in these difficult-to-treat cancers, and several groups have characterized EYA phosphatase inhibitors with the hope that they may be therapeutically useful. However, the molecular consequences of these drugs remain unknown as few EYA phosphatase substrates have been characterized. To better understand the function of EYAs, and the effect of their inhibition, we set out to identify EYA-substrate relationships with potential cancer promoting activity.
Methods/Results:
Using a combination of proximity proteomics, co-immunoprecipitation, co-localization, and mutational analysis, we identified Polo-like kinase 1 (PLK1) as a direct interactor of EYA1 and EYA4. Evidence from quantitative phosphoproteomics, in-vitro phosphatase assays and studies with phosphomutants indicates that PLK1 is a phosphatase substrate of EYA1 and EYA4, with pY445 and pY425 on PLK1 being the primary targets. EYA-mediated dephosphorylation of PLK1 enables PLK1 localization to mitotic structures and promotes the interaction between PLK1 and its activating cofactor BORA. Finally, either depletion of EYAs, or inhibition of EYA phosphatase activity, dramatically reduces PLK1 activation, causing significant mitotic cell death. These data demonstrate that PLK1 is an important target of EYA1 and EYA4 and implicates disruption of PLK1 activity by EYA phosphatase inhibition as a chemotherapeutic mechanism.
Conclusions:
We have identified and functionally characterised a potentially oncogenic mechanism whereby EYA1 and EYA4 promote cell division and survival through dephosphorylation of PLK1. Ongoing efforts involve establishing the therapeutic efficacy of an EYA phosphatase inhibitor in PDX models of high-risk neuroblastoma and determining the relative contribution of the EYA-PLK1 relationship to their growth and persistence