Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes

Ihsan Dereli; Vladyslav Telychko; Frantzeskos Papanikos; Kavya Raveendran; Jiaqi Xu; Michiel Boekhout; Marcello Stanzione; Benjamin Neuditschko; Naga Sailaja Imjeti; Elizaveta Selezneva; Hasibe Tuncay; Sevgican Demir; Teresa Giannattasio; Marc Gentzel; Anastasiia Bondarieva; Michelle Stevense; Marco Barchi; Arp Schnittger; John R Weir; Franz Herzog; Scott Keeney; Attila Tóth

doi:10.1038/s41467-024-47020-1

Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes

Ihsan Dereli, Vladyslav Telychko, Frantzeskos Papanikos, Kavya Raveendran, Jiaqi Xu, Michiel Boekhout, Marcello Stanzione, Benjamin Neuditschko, Naga Sailaja Imjeti, Elizaveta Selezneva, Hasibe Tuncay, Sevgican Demir, Teresa Giannattasio, Marc Gentzel, Anastasiia Bondarieva, Michelle Stevense, Marco Barchi, Arp Schnittger, John R Weir, Franz HerzogScott Keeney, Attila Tóth

Research output: Contribution to journal › Article › peer-review

Abstract

Programmed DNA double-strand break (DSB) formation is a unique meiotic feature that initiates recombination-mediated linking of homologous chromosomes, thereby enabling chromosome number halving in meiosis. DSBs are generated on chromosome axes by heterooligomeric focal clusters of DSB-factors. Whereas DNA-driven protein condensation is thought to assemble the DSB-machinery, its targeting to chromosome axes is poorly understood. We discovered in mice that efficient biogenesis of DSB-machinery clusters requires seeding by axial IHO1 platforms, which are based on a DBF4-dependent kinase (DDK)-modulated interaction between IHO1 and the chromosomal axis component HORMAD1. IHO1-HORMAD1-mediated seeding of the DSB-machinery on axes ensures sufficiency of DSBs for efficient pairing of homologous chromosomes. Without IHO1-HORMAD1 interaction, residual DSBs depend on ANKRD31, which enhances both the seeding and the growth of DSB-machinery clusters. Thus, recombination initiation is ensured by complementary pathways that differentially support seeding and growth of DSB-machinery clusters, thereby synergistically enabling DSB-machinery condensation on chromosomal axes.

Original language	English
Article number	2941
Pages (from-to)	2941
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-47020-1
Publication status	Published - 27 Nov 2023

Research fields

Cell Division
Proteomics
Mass spectrometry

IMC Research Focuses

Medical biotechnology

ÖFOS 2012 - Austrian Fields of Study

304005 Medical biotechnology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/s41467-024-47020-1

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Dereli, I., Telychko, V., Papanikos, F., Raveendran, K., Xu, J., Boekhout, M., Stanzione, M., Neuditschko, B., Imjeti, N. S., Selezneva, E., Tuncay, H., Demir, S., Giannattasio, T., Gentzel, M., Bondarieva, A., Stevense, M., Barchi, M., Schnittger, A., Weir, J. R., ... Tóth, A. (2023). Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes. Nature Communications, 15(1), 2941. Article 2941. https://doi.org/10.1038/s41467-024-47020-1

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title = "Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes",

abstract = "Programmed DNA double-strand break (DSB) formation is a unique meiotic feature that initiates recombination-mediated linking of homologous chromosomes, thereby enabling chromosome number halving in meiosis. DSBs are generated on chromosome axes by heterooligomeric focal clusters of DSB-factors. Whereas DNA-driven protein condensation is thought to assemble the DSB-machinery, its targeting to chromosome axes is poorly understood. We discovered in mice that efficient biogenesis of DSB-machinery clusters requires seeding by axial IHO1 platforms, which are based on a DBF4-dependent kinase (DDK)-modulated interaction between IHO1 and the chromosomal axis component HORMAD1. IHO1-HORMAD1-mediated seeding of the DSB-machinery on axes ensures sufficiency of DSBs for efficient pairing of homologous chromosomes. Without IHO1-HORMAD1 interaction, residual DSBs depend on ANKRD31, which enhances both the seeding and the growth of DSB-machinery clusters. Thus, recombination initiation is ensured by complementary pathways that differentially support seeding and growth of DSB-machinery clusters, thereby synergistically enabling DSB-machinery condensation on chromosomal axes.",

author = "Ihsan Dereli and Vladyslav Telychko and Frantzeskos Papanikos and Kavya Raveendran and Jiaqi Xu and Michiel Boekhout and Marcello Stanzione and Benjamin Neuditschko and Imjeti, {Naga Sailaja} and Elizaveta Selezneva and Hasibe Tuncay and Sevgican Demir and Teresa Giannattasio and Marc Gentzel and Anastasiia Bondarieva and Michelle Stevense and Marco Barchi and Arp Schnittger and Weir, {John R} and Franz Herzog and Scott Keeney and Attila T{\'o}th",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2023",

month = nov,

day = "27",

doi = "10.1038/s41467-024-47020-1",

language = "English",

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Dereli, I, Telychko, V, Papanikos, F, Raveendran, K, Xu, J, Boekhout, M, Stanzione, M, Neuditschko, B, Imjeti, NS, Selezneva, E, Tuncay, H, Demir, S, Giannattasio, T, Gentzel, M, Bondarieva, A, Stevense, M, Barchi, M, Schnittger, A, Weir, JR, Herzog, F, Keeney, S & Tóth, A 2023, 'Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes', Nature Communications, vol. 15, no. 1, 2941, pp. 2941. https://doi.org/10.1038/s41467-024-47020-1

TY - JOUR

T1 - Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes

AU - Dereli, Ihsan

AU - Telychko, Vladyslav

AU - Papanikos, Frantzeskos

AU - Raveendran, Kavya

AU - Xu, Jiaqi

AU - Boekhout, Michiel

AU - Stanzione, Marcello

AU - Neuditschko, Benjamin

AU - Imjeti, Naga Sailaja

AU - Selezneva, Elizaveta

AU - Tuncay, Hasibe

AU - Demir, Sevgican

AU - Giannattasio, Teresa

AU - Gentzel, Marc

AU - Bondarieva, Anastasiia

AU - Stevense, Michelle

AU - Barchi, Marco

AU - Schnittger, Arp

AU - Weir, John R

AU - Herzog, Franz

AU - Keeney, Scott

AU - Tóth, Attila

PY - 2023/11/27

Y1 - 2023/11/27

N2 - Programmed DNA double-strand break (DSB) formation is a unique meiotic feature that initiates recombination-mediated linking of homologous chromosomes, thereby enabling chromosome number halving in meiosis. DSBs are generated on chromosome axes by heterooligomeric focal clusters of DSB-factors. Whereas DNA-driven protein condensation is thought to assemble the DSB-machinery, its targeting to chromosome axes is poorly understood. We discovered in mice that efficient biogenesis of DSB-machinery clusters requires seeding by axial IHO1 platforms, which are based on a DBF4-dependent kinase (DDK)-modulated interaction between IHO1 and the chromosomal axis component HORMAD1. IHO1-HORMAD1-mediated seeding of the DSB-machinery on axes ensures sufficiency of DSBs for efficient pairing of homologous chromosomes. Without IHO1-HORMAD1 interaction, residual DSBs depend on ANKRD31, which enhances both the seeding and the growth of DSB-machinery clusters. Thus, recombination initiation is ensured by complementary pathways that differentially support seeding and growth of DSB-machinery clusters, thereby synergistically enabling DSB-machinery condensation on chromosomal axes.

AB - Programmed DNA double-strand break (DSB) formation is a unique meiotic feature that initiates recombination-mediated linking of homologous chromosomes, thereby enabling chromosome number halving in meiosis. DSBs are generated on chromosome axes by heterooligomeric focal clusters of DSB-factors. Whereas DNA-driven protein condensation is thought to assemble the DSB-machinery, its targeting to chromosome axes is poorly understood. We discovered in mice that efficient biogenesis of DSB-machinery clusters requires seeding by axial IHO1 platforms, which are based on a DBF4-dependent kinase (DDK)-modulated interaction between IHO1 and the chromosomal axis component HORMAD1. IHO1-HORMAD1-mediated seeding of the DSB-machinery on axes ensures sufficiency of DSBs for efficient pairing of homologous chromosomes. Without IHO1-HORMAD1 interaction, residual DSBs depend on ANKRD31, which enhances both the seeding and the growth of DSB-machinery clusters. Thus, recombination initiation is ensured by complementary pathways that differentially support seeding and growth of DSB-machinery clusters, thereby synergistically enabling DSB-machinery condensation on chromosomal axes.

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U2 - 10.1038/s41467-024-47020-1

DO - 10.1038/s41467-024-47020-1

M3 - Article

C2 - 38077023

SN - 2041-1723

VL - 15

SP - 2941

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 2941

ER -

Seeding the meiotic DNA break machinery and initiating recombination on chromosome axes

Abstract

Research fields

IMC Research Focuses

ÖFOS 2012 - Austrian Fields of Study

UN SDGs

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