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.

H2AT120ph H3T3ph PLK1 inner centromere lateral elements meiosis mouse

Journal

Frontiers in cell and developmental biology
ISSN: 2296-634X
Titre abrégé: Front Cell Dev Biol
Pays: Switzerland
ID NLM: 101630250

Informations de publication

Date de publication:
2022
Historique:
received: 14 10 2022
accepted: 19 12 2022
entrez: 3 2 2023
pubmed: 4 2 2023
medline: 4 2 2023
Statut: epublish

Résumé

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.

Identifiants

pubmed: 36733339
doi: 10.3389/fcell.2022.1069946
pii: 1069946
pmc: PMC9887526
doi:

Types de publication

Journal Article

Langues

eng

Pagination

1069946

Informations de copyright

Copyright © 2023 Gómez, Viera, Moreno-Mármol, Berenguer, Guajardo-Grence, Tóth, Parra and Suja.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Cell Div. 2018 Sep 19;13:7
pubmed: 30250494
EMBO Rep. 2014 Mar;15(3):273-81
pubmed: 24413556
J Cell Biol. 2012 Oct 15;199(2):251-68
pubmed: 23071152
Mol Cell. 2021 Jan 7;81(1):67-87.e9
pubmed: 33248027
Front Cell Dev Biol. 2017 Dec 22;5:112
pubmed: 29312936
J Cell Biol. 2007 Oct 22;179(2):255-67
pubmed: 17938250
Mol Cell Proteomics. 2011 Nov;10(11):M111.008540
pubmed: 21857030
Cell Cycle. 2020 Mar;19(6):625-641
pubmed: 31992120
PLoS Genet. 2020 Sep 15;16(9):e1009048
pubmed: 32931493
Cold Spring Harb Symp Quant Biol. 2010;75:419-23
pubmed: 21447816
EMBO J. 2017 Sep 1;36(17):2488-2509
pubmed: 28694245
J Cell Sci. 2003 Jul 1;116(Pt 13):2781-90
pubmed: 12759374
J Cell Biol. 2012 Oct 15;199(2):269-84
pubmed: 23071153
J Cell Sci. 2004 Mar 1;117(Pt 7):1221-34
pubmed: 14970259
Nat Cell Biol. 2001 Aug;3(8):761-6
pubmed: 11483963
Nat Commun. 2011 Sep 13;2:472
pubmed: 21915114
PLoS One. 2015 Feb 06;10(2):e0116783
pubmed: 25658810
Biol Reprod. 2018 Jul 1;99(1):112-126
pubmed: 29385397
Nat Struct Mol Biol. 2016 May 4;23(5):369-77
pubmed: 27142324
Exp Cell Res. 2010 Jan 15;316(2):158-71
pubmed: 19686734
Chromosome Res. 1997 Feb;5(1):66-8
pubmed: 9088645
Mol Carcinog. 2022 Feb;61(2):254-263
pubmed: 35049091
Elife. 2013 Nov 05;2:e01133
pubmed: 24192037
PLoS Genet. 2006 Jun 2;2(6):e84
pubmed: 16741559
Mol Cell Oncol. 2014 Oct 29;1(2):e954507
pubmed: 27308323
Curr Biol. 2004 Jul 13;14(13):1187-93
pubmed: 15242616
Science. 2010 Oct 8;330(6001):235-9
pubmed: 20705815
J Cell Biol. 1987 Jul;105(1):93-103
pubmed: 2440900
Nat Cell Biol. 2003 May;5(5):480-5
pubmed: 12717442
EMBO Rep. 2021 Apr 7;22(4):e51030
pubmed: 33615693
Chromosoma. 2014 Jun;123(3):239-52
pubmed: 24287868
Genes Dev. 2009 Sep 15;23(18):2237-51
pubmed: 19759266
EMBO Rep. 2021 Dec 6;22(12):e54106
pubmed: 34870374
EMBO Rep. 2007 Feb;8(2):173-80
pubmed: 17205076
Chromosome Res. 1998 Dec;6(8):639-42
pubmed: 10099877
Nature. 2015 Jan 22;517(7535):466-71
pubmed: 25533956
Biol Reprod. 2002 Aug;67(2):546-54
pubmed: 12135894
PLoS Genet. 2009 Oct;5(10):e1000702
pubmed: 19851446
J Cell Sci. 2012 Nov 1;125(Pt 21):5061-72
pubmed: 22854038
J Cell Sci. 2003 Mar 15;116(Pt 6):961-74
pubmed: 12584241
PLoS Genet. 2014 Feb 27;10(2):e1004194
pubmed: 24586209
Dev Biol. 2018 Feb 15;434(2):278-291
pubmed: 29269218
Genome Dyn. 2009;5:94-116
pubmed: 18948710
Asian J Androl. 2021 Nov-Dec;23(6):580-589
pubmed: 34528517
Genes Dev. 2008 Sep 1;22(17):2400-13
pubmed: 18765791
Mol Biol Cell. 2022 May 1;33(5):ar37
pubmed: 35274968
EMBO Rep. 2011 Mar;12(3):267-75
pubmed: 21274006
J Cell Biol. 2012 Dec 10;199(6):931-49
pubmed: 23209306
Mol Biol Cell. 2020 Jun 1;31(12):1206-1217
pubmed: 32267211
Science. 2010 Oct 8;330(6001):239-43
pubmed: 20929775
Genes (Basel). 2022 Mar 19;13(3):
pubmed: 35328099
PLoS Genet. 2019 Jan 3;15(1):e1007851
pubmed: 30605471
Cell Cycle. 2015;14(22):3566-79
pubmed: 26654596
Dev Cell. 2004 Feb;6(2):253-68
pubmed: 14960279
Genes Dev. 2010 Oct 1;24(19):2169-79
pubmed: 20889715
Trends Cell Biol. 2013 Apr;23(4):175-84
pubmed: 23246430
J Cell Biol. 1998 Jul 27;142(2):331-9
pubmed: 9679134
J Biol Chem. 2002 Nov 15;277(46):44115-20
pubmed: 12207013
J Cell Sci. 1994 Oct;107 ( Pt 10):2749-60
pubmed: 7876343
Nat Rev Mol Cell Biol. 2012 May 16;13(6):370-82
pubmed: 22588367
Science. 2010 Oct 8;330(6001):231-5
pubmed: 20705812
Cell Rep. 2016 Oct 18;17(4):977-986
pubmed: 27760328
FASEB J. 2012 Nov;26(11):4495-505
pubmed: 22859367
Cell. 2006 Jul 14;126(1):135-46
pubmed: 16839882
PLoS Genet. 2009 Mar;5(3):e1000417
pubmed: 19283064
EMBO J. 2011 Jul 08;30(15):3091-105
pubmed: 21743440
J Cell Biol. 2020 Apr 6;219(4):
pubmed: 32328639
J Cell Biol. 2009 Oct 19;187(2):185-99
pubmed: 19841137
Curr Biol. 2011 Jun 21;21(12):1061-9
pubmed: 21658950
J Cell Sci. 2022 Jul 1;135(13):
pubmed: 35694956
Curr Top Dev Biol. 2013;102:1-34
pubmed: 23287028
Mol Cell. 2006 Nov 3;24(3):409-22
pubmed: 17081991
PLoS One. 2007 Aug 22;2(8):e783
pubmed: 17712430
Curr Genet. 2019 Aug;65(4):817-827
pubmed: 30923890
Chromosoma. 1998 Dec;107(8):540-8
pubmed: 9933407
Oncogene. 2017 Aug 24;36(34):4819-4827
pubmed: 28436952
Mol Biol Cell. 2006 Aug;17(8):3705-16
pubmed: 16760428
Nat Rev Genet. 2010 Feb;11(2):124-36
pubmed: 20051984
J Cell Biol. 2003 Mar 3;160(5):657-70
pubmed: 12615909
PLoS Biol. 2005 Mar;3(3):e69
pubmed: 15737063
Genes Dev. 2008 Oct 1;22(19):2627-32
pubmed: 18832066
J Cell Sci. 2020 Dec 4;133(23):
pubmed: 33172986
Transl Oncol. 2022 Feb;16:101332
pubmed: 34973570
Science. 2010 Jan 8;327(5962):172-7
pubmed: 19965387
Genes Dev. 2005 Feb 15;19(4):472-88
pubmed: 15681610
Exp Cell Res. 2012 Jul 15;318(12):1340-6
pubmed: 22394509
Nat Commun. 2017 Sep 25;8(1):694
pubmed: 28947820
Curr Biol. 2007 Feb 20;17(4):304-15
pubmed: 17291761
J Cell Biol. 2020 Mar 2;219(3):
pubmed: 32027339
Curr Biol. 2007 Feb 20;17(4):316-22
pubmed: 17291758
J Cell Sci. 1999 Sep;112 ( Pt 17):2957-69
pubmed: 10444390
Trends Genet. 2018 Mar;34(3):232-245
pubmed: 29290403
Mol Cell. 2013 Dec 12;52(5):734-45
pubmed: 24184212
Chromosoma. 2002 Mar;111(1):53-61
pubmed: 12068923

Auteurs

Rocío Gómez (R)

Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.

Alberto Viera (A)

Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.

Tania Moreno-Mármol (T)

Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.

Inés Berenguer (I)

Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.
Departamento de Neuropatología Molecular, Centro de Biología Molecular Severo Ochoa, Campus de la Universidad Autónoma de Madrid, Madrid, Spain.

Andrea Guajardo-Grence (A)

Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.
Hospital Universitario Santa Cristina, Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa, Universidad Autónoma de Madrid, Madrid, Spain.

Attila Tóth (A)

Institute of Physiological Chemistry, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.

María Teresa Parra (MT)

Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.

José A Suja (JA)

Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain.

Classifications MeSH