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DNA damage signalling targets the kinetochore to promote chromatin mobility

Nature Cell Biology volume 18, pages 281–290 (2016)Cite this article

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Abstract

In budding yeast, chromatin mobility increases after a DNA double-strand break (DSB). This increase is dependent on Mec1, the yeast ATR kinase, but the targets responsible for this phenomenon are unknown. Here we report that the Mec1-dependent phosphorylation of Cep3, a kinetochore component, is required to stimulate chromatin mobility after DNA breaks. Cep3 phosphorylation counteracts a constraint on chromosome movement imposed by the attachment of centromeres to the spindle pole body. A second constraint, imposed by the tethering of telomeres to the nuclear periphery, is also relieved after chromosome breakage. A non-phosphorylatable Cep3 mutant that impairs DSB-induced chromatin mobility is proficient in DSB repair, suggesting that break-induced chromatin mobility may be dispensable for homology search. Rather, we propose that the relief of centromeric constraint promotes cell cycle arrest and faithful chromosome segregation through the engagement of the spindle assembly checkpoint.

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Figure 1: Relieving constraints on chromosomes mimics DSB-induced chromatin mobility.
Figure 2: Identification of a kinetochore component required for DSB-induced chromatin mobility.
Figure 3: Cep3 is a Rad53 phosphorylation target.
Figure 4: Cep3 modulates centromere attachment to the SPB.
Figure 5: Cep3 regulates the global chromatin response.
Figure 6: Centromeric constraint defines the increase in DSB-induced mobility.
Figure 7: Cep3 phosphorylation promotes cell cycle arrest and genome stability.
Figure 8: Proposed model for Cep3 following a DSB.

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Acknowledgements

We are grateful to R. Szilard and members of the Durocher laboratory for critical reading of the manuscript. We also thank S. Jaspersen (Stowers Institute for Medical Research, USA), P. Hieter (University of British Columbia, Canada), G. Brown (University of Toronto, Canada), M. Meneghini (University of Toronto, Canada), R. Rothstein (Columbia University, USA), S. Gasser (Friedrich Miescher Institute, Switzerland), S. Biggins (Fred Hutchinson Cancer Research Center, USA) and M. Kupiec (Tel Aviv University, Israel) for sharing strains and plasmids. J.S. is supported by a CIHR Doctoral award. D.D. is the Thomas Kierans Chair in Mechanisms of Cancer Development and a Canada Research Chair (Tier 1) in the Molecular Mechanisms of Genome Integrity. This work was supported by CIHR grant FDN143343 (to D.D.) and MOP123468 (to L.P.) and a Grant-in-Aid from the Krembil Foundation to L.P. and D.D.

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Authors and Affiliations

  1. Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, Ontario M5G 1X5, Canada

    Jonathan Strecker, Gagan D. Gupta, Mikhail Bashkurov, Marie-Claude Landry, Laurence Pelletier & Daniel Durocher

  2. Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 3E1, Canada

    Jonathan Strecker, Wei Zhang, Laurence Pelletier & Daniel Durocher

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Contributions

J.S. carried out the experiments and wrote the manuscript. G.D.G. and M.B. generated MATLAB scripts for nuclear alignment and MSD analysis. W.Z. and M.-C.L. helped initiate the project and set up the microscopy system for measuring chromatin mobility. L.P. supervised G.D.G. and M.B. and provided microscopy advice. D.D. supervised the project and wrote the manuscript with J.S.

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Correspondence to Daniel Durocher.

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Integrated supplementary information

Supplementary Figure 3 System for chromatin mobility analysis in budding yeast.

(a) Representative images of mobility strains. Chromatin is tracked by integrating LacOx256 arrays in cells expressing LacI-GFP and Nup49-mCherry. Scale bar represents 2 μm. (b) X-axis displacement of a single tracked MAT locus over time in 1 × 1 or 2 × 2 binned images. (c) Growth comparison of unexposed and imaged cells. Cells were held in a DeltaVision microscope at 30 °C in SD media supplemented with raffinose and imaged at the indicated time points. Scale bar represents 4 μm. (d) MSD analysis of the MAT locus in wild-type cells before and 3 h after DSB induction. (e) MSD analysis of the MAT locus in wild-type cells or in the INO80 mutant arp8Δ. All MSD data represent the mean ± s.e.m. of cells pooled from 3 independent experiments. See Supplementary Table 1 for mobility parameters and the precise number of cells analysed.

Supplementary Figure 4 Cep3-S575 is required for DSB-induced chromatin mobility.

(a,b) Radius of confinement (a) and diffusion coefficients (b) of wild-type and cep3-S575A cells following a DSB. Data represents the mean ± s.e.m., n represent the number of cells pooled from 3 independent experiments (WT control n = 131, WT DSB n = 81, cep3-S575A control n = 189, cep3-S575A DSB n = 111). ∗∗∗P < 0.001; one-way ANOVA. (c) MSD analysis of the MAT locus in wild-type cells and a cep3-S575A mutant generated at the endogenous CEP3 locus by the pop-in/pop-out method. (d) MSD analysis of the MAT locus in wild-type or cep3-S575A/cep3-S575A diploid cells containing an HO cut site on one homolog. All MSD data represent the mean ± s.e.m. of cells pooled from 3 independent experiments. See Supplementary Table 1 for mobility parameters and the precise number of cells analysed.

Supplementary Figure 5 Cep3 phosphorylation requires Mec1/Rad53/Dun1 signalling.

(a) Immunoblot analysis using a Cep3-S575 phosphospecific antibody on whole cell extracts from cells expressing Myc-tagged Cep3 (WT or S575A) in response to a HO-induced DSB. Rad53 was probed to confirm checkpoint activation, Myc was used to control for loading. (b) Immunoblot analysis of asynchronous (ASN), α-factor arrested (G1, or nocodazole arrested (G2/M) cells treated with Zeocin (250 μg ml−1) for 1 h. Levels of the mitotic cyclin Clb2 were ascertained to confirm cell cycle synchronization. Pgk1 and Rad53 were probed to control for loading and to confirm checkpoint activation respectively. (c) MSD analysis of the MAT locus in sml1Δ tel1Δ mutants. (d) MSD analysis of the MAT locus in sml1Δ tel1Δ mec1Δ mutants. (e) MSD analysis of the MAT locus in cep3-S575A rad53Δ mutants. (f) Amino acid sequence surrounding Cep3-S575 and the consensus phosphorylation target sites of the Rad53 and Dun1 kinases. Matching residues are highlighted in red, Ψ represents aliphatic amino acids. (g) Time-course of Cep3-13xMyc phosphorylation in response to Zeocin (250 μg ml−1) determined by immunoblot analysis. (h) MSD analysis of the MAT locus in dun1Δ mutants. (i) Cep3-S575 phosphorylation in dun1Δ cells following 1 h of Zeocin treatment (250 μg ml−1) determined by immunoblot analysis.

Supplementary Figure 6 Mobility of a CEN-bound episome following DSB induction.

(a,b) MSD analysis of a CEN/ARS-LacOx256 episome in wild-type (a) and cep3-S575A (b) cells in response to a DSB 27 kb from CEN4. (c) MSD analysis of a CEN/ARS-LacOx256 episome in response to a DSB 998 kb from CEN4. All MSD data represent the mean ± s.e.m. of cells pooled from 3 independent experiments. See Supplementary Table 1 for mobility parameters and the precise number of cells analysed.

Supplementary Figure 7 Loss of telomeric tethering does not increase the mobility of a broken chromosome arm.

(a) MSD analysis of the MAT locus on Chr III (in cis) and the MAK10 locus on unbroken Chr V in trans to a DSB 27 kb from CEN4. (b) MSD analysis of the MAK10 locus on unbroken Chr V in trans to a DSB 27 kb from CEN4 in sir4Δ cells. (c,d,e) MSD analysis of the MAT locus, in cis to a DSB, in sir4Δ (c), yku70Δ (d), and yku70Δ sir4Δ (e) cells. All MSD data represent the mean ± s.e.m. of cells pooled from 3 independent experiments. See Supplementary Table 1 for mobility parameters and the precise number of cells analysed.

Supplementary Figure 8 Mobility of a broken and unbroken chromosome arm.

(a) Schematic of strains to follow the mobility of both chromosome arms following an HO-induced DSB on Chr IV (red triangle). (b) MSD analysis of the Chr IV-R and Chr IV-L arms before and after a DSB. (c) MSD analysis of the uncut Chr IV-L arm in wild-type and cep3-S575A cells. (d) MSD analysis of the cut Chr IV-R arm and the uncut Chr IV-L arm after a DSB in a sir4Δ background. All MSD data represent the mean ± s.e.m. of cells pooled from 3 independent experiments. See Supplementary Table 1 for mobility parameters and the precise number of cells analysed.

Supplementary Figure 9 Cep3-S75A does not affect the kinetics of DSB repair or DNA binding.

(a) Schematic of the HR repair strain NA60. PCR primers P1 and P2 were used to amplify the homologous recombination cassette containing the HO cut site on Chr IX. Repair of the DSB by HR is accompanied by the appearance of a ClaI site provided by the donor recombination cassette on Chr XIII. (b) Agarose gel of ClaI-digested PCR products in response to a DSB in wild-type and cep3-S575A cells. DNA was extracted from cells harvested at the indicated time points, the cut locus was amplified by PCR, and PCR products were digested with ClaI. Gene conversion (GC) products are cleaved by ClaI and form two lower molecular weight bands. Early repair products can be detected at 2.5 h in both wild-type and cep3-S575A cells. A colony that survived plating on galactose was used as a positive control (+). (c) Chromatin immunoprecipitation (ChIP) of Cep3-13xMyc and Cep3-S575A-13xMyc in response to a DSB at the MAT locus. Fold enrichment at CEN3 is normalized to the non-centromeric control locus TSC11. Data represents the mean ± s.d., n = 5 independent experiments for each condition.

Supplementary Figure 10 Cep3 and INO80 function in a common pathway.

(a,b) MSD analysis of the MAT locus in INO80 mutant arp8Δ cells with CEN3 (a) or CEN5 (b) inactivation. (c) Length of checkpoint arrest in response to an irreparable DSB at the MAT locus. Each dot represents a single cell combined from 2 or more independent experiments for each genotype (WT n = 199 cells, cep3-S575A n = 194, arp8Δ n = 171, cep3-S75A arp8Δ n = 171); red bars represent the median arrest length. (d) Immunoblot analysis of Cep3-S575 phosphorylation in wild-type and cep3-S575Acells, and two clones each of the INO80 mutants arp5Δ and arp8Δ after Zeocin treatment (250 μg ml−1) for 1 h (+) as described in Fig. 3c. All MSD data represent the mean ± s.e.m. of cells pooled from 3 independent experiments. See Supplementary Table 1 for mobility parameters and the precise number of cells analysed.

Supplementary Figure 11 Uncropped scans of immunoblots.

Cropped images for figures are indicated by a red box.

Supplementary Table 1 Summary of mobility parameters.
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Supplementary Table 2 Strains used in this study.
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Strecker, J., Gupta, G., Zhang, W. et al. DNA damage signalling targets the kinetochore to promote chromatin mobility. Nat Cell Biol 18, 281–290 (2016). https://doi.org/10.1038/ncb3308

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