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Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1

Nature Cell Biology volume 13, pages 599–610 (2011)Cite this article

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Abstract

Meiotic crossover formation between homologous chromosomes (homologues) entails DNA double-strand break (DSB) formation, homology search using DSB ends, and synaptonemal-complex formation coupled with DSB repair. Meiotic progression must be prevented until DSB repair and homologue alignment are completed, to avoid the formation of aneuploid gametes. Here we show that mouse HORMAD1 ensures that sufficient numbers of processed DSBs are available for successful homology search. HORMAD1 is needed for normal synaptonemal-complex formation and for the efficient recruitment of ATR checkpoint kinase activity to unsynapsed chromatin. The latter phenomenon was proposed to be important in meiotic prophase checkpoints in both sexes. Consistent with this hypothesis, HORMAD1 is essential for the elimination of synaptonemal-complex-defective oocytes. Synaptonemal-complex formation results in HORMAD1 depletion from chromosome axes. Thus, we propose that the synaptonemal complex and HORMAD1 are key components of a negative feedback loop that coordinates meiotic progression with homologue alignment: HORMAD1 promotes homologue alignment and synaptonemal-complex formation, and synaptonemal complexes downregulate HORMAD1 function, thereby permitting progression past meiotic prophase checkpoints.

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Figure 1: HORMAD1 promotes synaptonemal-complex formation independently of DSB-dependent processes.
Figure 2: Numbers of early-, intermediate- and late-recombination-protein foci are lower in the absence of HORMAD1 in prophase meiocytes.
Figure 3: Amounts of SPO11–oligonucleotide complexes in testes are lower in the absence of HORMAD1.
Figure 4: HORMAD1 is required for sex-body and pseudo-sex-body formation in the Spo11+/+ and Spo11−/− backgrounds, respectively.
Figure 5: HORMAD1 is required for efficient accumulation of ATR, TOPBP1 and BRCA1 on chromatin in the absence of programmed DSBs.
Figure 6: Lack of HORMAD1 allows survival of oocytes in the synaptonemal-complex-defective Spo11−/− mutant.
Figure 7: Lower numbers of chiasmata form in Hormad1−/− oocytes.
Figure 8: Model for meiotic progression: negative feedback loop of HORMAD1 and synaptonemal-complex coordinates homology search and meiotic progression.

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Acknowledgements

We thank A. Hientzsch and K. Duerschke for general laboratory support and technical assistance; R. Jessberger for sharing ideas, antibodies (anti-SYCP3, anti-STAG3 and anti-SMC3) and support; F. Baudat and B. De Massy for providing us with Spo11+/− mice; J. Chen for the anti-TOPBP1 antibody; E. Marcon for the anti-RPA antibody; C. Höög for anti-SYCE1 and anti-SYCE2 antibodies; G.C. Enders for the anti-GCNA antibody; and M.P. Thelen for the anti-SPO11 antibody. We are grateful to M. Siomos and D. Knapp for discussion, revising and proofreading the manuscript. The Deutsche Forschungsgemeinschaft (DFG; grants: TO421/4-1 SPP1384 and TO421/3-1) and the Sächsisches Staatsministerium für Wissenschaft und Kunst supported K.D. and A.T.; Grants HD53855 and HD40916 from the US National Institutes of Health supported J.L., I.R., M.J. and S.K.; ARC (Subvention fixe 1143) and La Ligue Regionale (RS09/75-39) supported K.H. and K.W.; the Medical Research Council UK supported H.J.C.; the DFG research centre and cluster of excellence to the Center for Regenerative Therapies Dresden (CRTD) supported the work of K.A.; a CRTD seed grant supported K.A. and A.T.; and an EFRE grant (Europäischer Fonds für Regionale Entwicklung) supported K.A., J.F. and A.F.S.

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  1. Ignasi Roig

    Present address: Present address: Unitat de Citologia i Histologia, Departamento Biologia Cellular, Fisiologia i Immunologia, Facultat de Biociències, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, 08193, Spain,

Authors and Affiliations

  1. Institute of Physiological Chemistry, Technische Universität Dresden, Fiedlerstrasse 42, 01307 Dresden, Germany

    Katrin Daniel & Attila Tóth

  2. Molecular Biology Program, Memorial Sloan-Kettering Cancer Center, New York, New York 10065, USA

    Julian Lange, Ignasi Roig & Scott Keeney

  3. CNRS UMR7622 Biologie du Développement, 9 quai St Bernard, Paris, 75005, France

    Khaled Hached & Katja Wassmann

  4. UPMC Paris 6, 9 quai St Bernard, Paris, 75005, France

    Khaled Hached & Katja Wassmann

  5. Genomics, BioInnovationsZentrum, Technische Universität Dresden, Am Tatzberg 47, 01307 Dresden, Germany

    Jun Fu & A. Francis Stewart

  6. Center for Regenerative Therapies Dresden, BioInnovationsZentrum, Technische Universität Dresden, Am Tatzberg 47, 01307 Dresden, Germany

    Konstantinos Anastassiadis

  7. MRC Human Genetics Unit, Western General Hospital, Crewe Road, Edinburgh, EH4 2XU, UK

    Howard J. Cooke

  8. Developmental Biology Program, Memorial Sloan-Kettering Cancer Center, New York, New York 10065, USA

    Maria Jasin

  9. Howard Hughes Medical Institute, Memorial Sloan-Kettering Cancer Center, New York, New York 10065, USA

    Scott Keeney

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Contributions

K.D. designed, carried out and analysed most of the experiments; J.L., I.R., M.J. and S.K. contributed with SPO11–oligonucleotide measurements; J.F., K.A. and A.F.S. designed and generated the targeting construct and targeted embryonic stem cells; K.H. and K.W. carried out oocyte-maturation experiments and oocyte video microscopy; H.J.C. provided the

Syce2+/− mouse, A.T. was involved in oocyte-maturation experiments and oocyte counts, helped K.D. in experimental design and wrote the paper together with K.D. All authors were involved in discussions and commented on the manuscript.

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Correspondence to Ignasi Roig or Attila Tóth.

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Daniel, K., Lange, J., Hached, K. et al. Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 13, 599–610 (2011). https://doi.org/10.1038/ncb2213

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