Cargando…

The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis

Asymmetric disassembly of the synaptonemal complex (SC) is crucial for proper meiotic chromosome segregation. However, the signaling mechanisms that directly regulate this process are poorly understood. Here we show that the mammalian Rho GEF homolog, ECT-2, functions through the conserved RAS/ERK M...

Descripción completa

Detalles Bibliográficos
Autores principales: Nadarajan, Saravanapriah, Mohideen, Firaz, Tzur, Yonatan B, Ferrandiz, Nuria, Crawley, Oliver, Montoya, Alex, Faull, Peter, Snijders, Ambrosius P, Cutillas, Pedro R, Jambhekar, Ashwini, Blower, Michael D, Martinez-Perez, Enrique, Harper, J Wade, Colaiacovo, Monica P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4805554/
https://www.ncbi.nlm.nih.gov/pubmed/26920220
http://dx.doi.org/10.7554/eLife.12039
_version_ 1782423156980449280
author Nadarajan, Saravanapriah
Mohideen, Firaz
Tzur, Yonatan B
Ferrandiz, Nuria
Crawley, Oliver
Montoya, Alex
Faull, Peter
Snijders, Ambrosius P
Cutillas, Pedro R
Jambhekar, Ashwini
Blower, Michael D
Martinez-Perez, Enrique
Harper, J Wade
Colaiacovo, Monica P
author_facet Nadarajan, Saravanapriah
Mohideen, Firaz
Tzur, Yonatan B
Ferrandiz, Nuria
Crawley, Oliver
Montoya, Alex
Faull, Peter
Snijders, Ambrosius P
Cutillas, Pedro R
Jambhekar, Ashwini
Blower, Michael D
Martinez-Perez, Enrique
Harper, J Wade
Colaiacovo, Monica P
author_sort Nadarajan, Saravanapriah
collection PubMed
description Asymmetric disassembly of the synaptonemal complex (SC) is crucial for proper meiotic chromosome segregation. However, the signaling mechanisms that directly regulate this process are poorly understood. Here we show that the mammalian Rho GEF homolog, ECT-2, functions through the conserved RAS/ERK MAP kinase signaling pathway in the C. elegans germline to regulate the disassembly of SC proteins. We find that SYP-2, a SC central region component, is a potential target for MPK-1-mediated phosphorylation and that constitutively phosphorylated SYP-2 impairs the disassembly of SC proteins from chromosomal domains referred to as the long arms of the bivalents. Inactivation of MAP kinase at late pachytene is critical for timely disassembly of the SC proteins from the long arms, and is dependent on the crossover (CO) promoting factors ZHP-3/RNF212/Zip3 and COSA-1/CNTD1. We propose that the conserved MAP kinase pathway coordinates CO designation with the disassembly of SC proteins to ensure accurate chromosome segregation. DOI: http://dx.doi.org/10.7554/eLife.12039.001
format Online
Article
Text
id pubmed-4805554
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-48055542016-03-25 The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis Nadarajan, Saravanapriah Mohideen, Firaz Tzur, Yonatan B Ferrandiz, Nuria Crawley, Oliver Montoya, Alex Faull, Peter Snijders, Ambrosius P Cutillas, Pedro R Jambhekar, Ashwini Blower, Michael D Martinez-Perez, Enrique Harper, J Wade Colaiacovo, Monica P eLife Cell Biology Asymmetric disassembly of the synaptonemal complex (SC) is crucial for proper meiotic chromosome segregation. However, the signaling mechanisms that directly regulate this process are poorly understood. Here we show that the mammalian Rho GEF homolog, ECT-2, functions through the conserved RAS/ERK MAP kinase signaling pathway in the C. elegans germline to regulate the disassembly of SC proteins. We find that SYP-2, a SC central region component, is a potential target for MPK-1-mediated phosphorylation and that constitutively phosphorylated SYP-2 impairs the disassembly of SC proteins from chromosomal domains referred to as the long arms of the bivalents. Inactivation of MAP kinase at late pachytene is critical for timely disassembly of the SC proteins from the long arms, and is dependent on the crossover (CO) promoting factors ZHP-3/RNF212/Zip3 and COSA-1/CNTD1. We propose that the conserved MAP kinase pathway coordinates CO designation with the disassembly of SC proteins to ensure accurate chromosome segregation. DOI: http://dx.doi.org/10.7554/eLife.12039.001 eLife Sciences Publications, Ltd 2016-02-27 /pmc/articles/PMC4805554/ /pubmed/26920220 http://dx.doi.org/10.7554/eLife.12039 Text en © 2016, Nadarajan et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Nadarajan, Saravanapriah
Mohideen, Firaz
Tzur, Yonatan B
Ferrandiz, Nuria
Crawley, Oliver
Montoya, Alex
Faull, Peter
Snijders, Ambrosius P
Cutillas, Pedro R
Jambhekar, Ashwini
Blower, Michael D
Martinez-Perez, Enrique
Harper, J Wade
Colaiacovo, Monica P
The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis
title The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis
title_full The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis
title_fullStr The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis
title_full_unstemmed The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis
title_short The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis
title_sort map kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4805554/
https://www.ncbi.nlm.nih.gov/pubmed/26920220
http://dx.doi.org/10.7554/eLife.12039
work_keys_str_mv AT nadarajansaravanapriah themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT mohideenfiraz themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT tzuryonatanb themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT ferrandiznuria themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT crawleyoliver themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT montoyaalex themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT faullpeter themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT snijdersambrosiusp themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT cutillaspedror themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT jambhekarashwini themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT blowermichaeld themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT martinezperezenrique themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT harperjwade themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT colaiacovomonicap themapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT nadarajansaravanapriah mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT mohideenfiraz mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT tzuryonatanb mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT ferrandiznuria mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT crawleyoliver mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT montoyaalex mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT faullpeter mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT snijdersambrosiusp mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT cutillaspedror mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT jambhekarashwini mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT blowermichaeld mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT martinezperezenrique mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT harperjwade mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis
AT colaiacovomonicap mapkinasepathwaycoordinatescrossoverdesignationwithdisassemblyofsynaptonemalcomplexproteinsduringmeiosis