Kinase PLK1 regulates the disassembly of the lateral elements and the assembly of the inner centromere during the diakinesis/metaphase I transition in male mouse meiosis

Rocío Gómez; Alberto Viera; Tania Moreno-Mármol; Inés Berenguer; Andrea Guajardo-Grence; Attila Tóth; María Teresa Parra; José A Suja

doi:10.3389/fcell.2022.1069946

Kinase PLK1 regulates the disassembly of the lateral elements and the assembly of the inner centromere during the diakinesis/metaphase I transition in male mouse meiosis

Front Cell Dev Biol. 2023 Jan 13:10:1069946. doi: 10.3389/fcell.2022.1069946. eCollection 2022.

Authors

Rocío Gómez¹, Alberto Viera¹, Tania Moreno-Mármol¹, Inés Berenguer^{1

2}, Andrea Guajardo-Grence^{1

3}, Attila Tóth⁴, María Teresa Parra¹, José A Suja¹

Affiliations

¹ Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.
² Departamento de Neuropatología Molecular, Centro de Biología Molecular Severo Ochoa, Campus de la Universidad Autónoma de Madrid, Madrid, Spain.
³ Hospital Universitario Santa Cristina, Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa, Universidad Autónoma de Madrid, Madrid, Spain.
⁴ Institute of Physiological Chemistry, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.

Abstract

PLK1 is a serine/threonine kinase with crucial roles during mitosis. However, its involvement during mammalian male meiosis remains largely unexplored. By inhibiting the kinase activity of PLK1 using BI 2536 on organotypic cultures of seminiferous tubules, we found that the disassembly of SYCP3 and HORMAD1 from the lateral elements of the synaptonemal complex during diakinesis is impeded. We also found that the normal recruitment of SYCP3 and HORMAD1 to the inner centromere in prometaphase I spermatocytes did not occur. Additionally, we analyzed the participation of PLK1 in the assembly of the inner centromere by studying its implication in the Bub1-H2AT120ph-dependent recruitment of shugoshin SGO2, and the Haspin-H3T3ph-dependent recruitment of Aurora B/C and Borealin. Our results indicated that both pathways are regulated by PLK1. Altogether, our results demonstrate that PLK1 is a master regulator of the late prophase I/metaphase I transition in mouse spermatocytes.

Keywords: H2AT120ph; H3T3ph; PLK1; inner centromere; lateral elements; meiosis; mouse.

Grants and funding

This work was supported by funding from Ministerio de Ciencia e Innovación (Spain) grant PID2020-117491GB-I00 (to JS). TM-M was supported by grant “Ayuda para Inicio de Estudios en Programas de Posgrado” from Universidad Autónoma de Madrid (Spain). IB was supported by an FPI predoctoral fellowship from Ministerio de Economía y Competitividad (Spain). AG-G was supported by grant “Ayuda para el Fomento de la Investigación en Estudios de Máster,” and “Ayudas PostMáster from the Department of Biology at Universidad Autónoma de Madrid.