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Cellular response upon proliferation in the presence of an active mitotic checkpoint

Andrea Corno, Elena Chiroli, Fridolin Gross, Claudio Vernieri, Vittoria Matafora, View ORCID ProfileStefano Maffini, Marco Cosentino Lagomarsino, View ORCID ProfileAngela Bachi, View ORCID ProfileAndrea Ciliberto  Correspondence email
Andrea Corno
1Istituto Firc di Oncologia Molecolare, Milan, Italy
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Elena Chiroli
1Istituto Firc di Oncologia Molecolare, Milan, Italy
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Fridolin Gross
1Istituto Firc di Oncologia Molecolare, Milan, Italy
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Claudio Vernieri
1Istituto Firc di Oncologia Molecolare, Milan, Italy
2Medical Oncology Department, Fondazione IRCCS Istituto Nazionale Tumori, Milan, Italy
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Vittoria Matafora
1Istituto Firc di Oncologia Molecolare, Milan, Italy
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Stefano Maffini
3Department of Mechanistic Cell Biology, Max Planck Institute of Molecular Physiology, Dortmund, Germany
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Marco Cosentino Lagomarsino
1Istituto Firc di Oncologia Molecolare, Milan, Italy
4Physics Department, University of Milan, Milan, Italy
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Angela Bachi
1Istituto Firc di Oncologia Molecolare, Milan, Italy
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Andrea Ciliberto
1Istituto Firc di Oncologia Molecolare, Milan, Italy
5Istituto di Genetica Molecolare, Consiglio Nazionale delle Ricerche, Pavia, Italy
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  • For correspondence: andrea.ciliberto@ifom.eu
Published 8 May 2019. DOI: 10.26508/lsa.201900380
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  • Figure 1.
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    Figure 1. Single-cell analysis of proliferating cells in the presence of an active mitotic checkpoint.

    (A) Schematics of the two strategies for inducing the mitotic checkpoint: perturbing the mitotic spindle (tub2-401 grown at low temperatures, left) or inducing Mad2 overexpression (GAL1-MAD2, right). (B) Quantities measured in single-cell analysis. Budding marks the G1/S transition, increasing and decreasing levels of Clb2 correspond, respectively, to prometaphase and anaphase onset. (C–E) Cells were synchronized in G1 and released in the presence of galactose (yAC2006: CLB2-GFP TUB2-mCherry; yAC2671: CLB2-GFP TUB2-mCherry GAL1-MAD2) or at the semi-permissive temperature. C (yAC3491: CLB2-GFP, yAC2970: CLB2-GFP, tub2-401). (C) Example of Clb2-GFP trajectories for GAL1-MAD2 cells (on the left) and for tub2-401 cells (on the right). For Mad2-overexpressing cells, we compared cells dividing with an active checkpoint (SAC-active) to CLB2-GFP TUB2-mCherry released from the arrest and dividing in galactose (unperturbed). When instead the checkpoint was induced by the temperature-sensitive β-tubulin mutant, SAC-active tub2-401 CLB2-GFP cells were released from the G1 arrest at the semi-permissive temperature. CLB2-GFP grown at the semipermissive temperature were the unperturbed cells. (D, E) Distributions of cell cycle lengths and mitotic lengths for unperturbed and SAC-active cells under the two experimental conditions. N, number of observations; m, median of the distribution. Censored data (i.e., dead cells or precocious end of cell monitoring) were represented as white circles. Significant differences between unperturbed and SAC-active cells were evaluated with a log-rank test (significance level: 0.05).

  • Figure S1.
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    Figure S1. related with Fig 1—Controls of cell division under checkpoint activating conditions.

    (A) WT (yAC3997) and tub2-401 (yAC3927) cells were synchronized in G1 with α-factor and released at either 22°C or 15°C. After 24 h, the cells were sampled and stained for DNA content (DAPI) and α-tubulin Tub1 (FITC) by immunofluorescence. Scale bar: 5 μm. (B) Spotting of serial dilutions of WT (yAC3568), mad2Δ (yAC3372), tub2-401 (yAC3220), and tub2-401 mad2Δ (yAC2946) cells on YEPD plates incubated at 30°C, 22°C, and 15°C. (C) Spotting of serial dilutions of WT (yAC1001) and GAL1-MAD2 (yAC2465) cells on YEPD plate (no Mad2 overexpression) and YEPRG plate (Mad2 overexpression). (D) Evaluation of mis-segregation events. WT (yAC4013), GAL1-MAD2 (yAC4018), and tub2-401 (yAC4012) cells carrying Htb2-mCherry and ChrV-GFP were synchronized in G1 and released, respectively, in YEPRG at 30°C and YEPD at 22°C. After 24 h from G1 release, the samples were collected and imaged. Left panel: examples of mis-segregating cells (pointed by the arrow). Scale bar: 5 μm. Central panel: percentages of cells with ChrV mis-segregation for each condition. Biological replicate #1 (black circle): WT [YEPRG] 0% (0/66); GAL1-MAD2 [YEPRG] 2.20% (2/91); WT [22°C] 0% (0/67); tub2-401 [22°C] 4.65% (6/129). Biological replicate #2 (red circle): WT [YEPRG] 0% (0/105); GAL1-MAD2 [YEPRG] 2.27% (3/132); WT [22°C] 0% (0/140); tub2-401 [22°C] 6.72% (16/238). Right panel: estimation of the probability of having at least one aneuploid chromosome as a function of the ChrV mis-segregation rates. Blue line represents the theoretical function of the probability—see the Materials and Methods section for details—and dots are representative of the biological replicates in the central panel.

  • Figure S2.
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    Figure S2. related with Fig 1—Single-cell properties of SAC-active cells.

    (A) Definition of unperturbed and SAC-active cells. The first generation (i.e., gen0) has been evaluated from α-factor release and rebudding, whereas subsequent cell cycles (i.e., gen1, gen2, …) from budding to rebudding. Unperturbed cells correspond to WT cells, whereas SAC-active refers to GAL1-MAD2 or tub2-401 cells. (B) Description of the monitored GAL1-MAD2 and tub2-401 SAC-active cells up to generation 1. Proportion of censored and uncensored event were reported for each biological replicate. (C) SAC-active tub2-401 cells are delayed in mitosis because of an active SAC. Unperturbed CLB2-GFP (yAC3491), SAC-active CLB2-GFP tub2-401 (yAC2970), and SAC-deficient CLB2-GFP tub2-401 mad2Δ (yAC3034) cells were synchronized in G1 and released at the semipermissive temperature. Mitotic length of gen0 was evaluated for each condition. N, number of observations; m, median of the distribution. Censored data (i.e., dead cells or precocious end of cell monitoring) are represented as white circles. (D) Evaluation of maximum levels of nuclear Clb2 during the mitosis of unperturbed and SAC-active cells. The maximum value of Clb2 trajectory was measured for each mitotic length of unperturbed and SAC-active cells. N: number of observations; m: median of the distribution. Significant differences between unperturbed and SAC-active cells were evaluated with a two-sample t test with unequal variances or Wilcoxon rank sum test (significance level: 0.05), respectively, according to the normality or not of the distributions. (E) Distributions of Clb2 levels after Clb2 degradation in unperturbed and SAC-active cells at gen0. For each cell, mean cytoplasmic levels of Clb2 were measured from anaphase onset to rebudding, and the minimum value within this interval was evaluated. Number of observations for GAL1-MAD2: unperturbed gen0: 54; SAC-active gen0: 45. Number of observations for tub2-401: unperturbed gen0: 72; SAC-active gen0: 78. (F, G) Evaluation of cell cycle and mitotic length of SAC-active cells clustered by the number of generations after gen0. N, number of observations; m, median of the distribution. Censored data were represented as white circles.

  • Figure 2.
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    Figure 2. Deletion of CDH1 impairs the proliferation of SAC-active cells.

    (A) Spotting of serial dilutions of WT (yAC3568), cdh1Δ (yAC1533), SIC1(10x) (yAC3650), cdh1Δ SIC1(10x) (yAC3683), GAL1-MAD2 (yAC2465), GAL1-MAD2 cdh1Δ (yAC3582), GAL1-MAD2 SIC1(10x) (yAC3654), and GAL1-MAD2 cdh1Δ SIC1(10x) (yAC3659) on YEPD plate (without Mad2 overexpression) or YEPRG plate (with Mad2 overexpression). (B) Spotting of serial dilution of WT (yAC3568), cdh1Δ (yAC1533), SIC1(10x) (yAC3650), cdh1Δ SIC1(10x) (yAC3683), tub2-401 (yAC3220), tub2-401 cdh1Δ (yAC3686), tub2-401 SIC1(10x) (yAC3685), and tub2-401 cdh1Δ SIC1(10x) (yAC3694) on YEPD plates incubated at 30°, 20°, and 18°C. (C, D) Single-cell analysis of GAL1-MAD2 cdh1Δ SAC-active cells. Proliferation of GAL1-MAD2 (yAC3883) and GAL1-MAD2 cdh1Δ (yAC3885) cells carrying Htb2-mCherry and Clb2-GFP was monitored in microfluidic chamber, in the continuous presence of YEPRG medium. (C) Clb2 trajectories were synchronized in silico at the beginning of Clb2 degradation in the first division upon Mad2 overexpression. Individual traces of Clb2 are reported as thin lines, their mean trajectory as thick lines. N, number of trajectories. (D) Duration of cell cycle length and anaphase-to-G1 in SAC-active cells. Nuclear segregation was used to identify anaphase onset. N, number of observations; m, median of the distribution. Censored data (i.e., dead cells or precocious end of cell monitoring) are represented as white circles. Significant differences between GAL1-MAD2 and GAL1-MAD2 cdh1Δ cells were evaluated with a log-rank test (significance level: 0.05).

  • Figure S3.
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    Figure S3. related with Fig 2—Cell cycle dynamics in cdh1Δ cells.

    (A) Mitotic length of GAL1-MAD2 and GAL1-MAD2 cdh1Δ cells during the first mitotic arrest. Nuclear segregation was the readout of anaphase onset. N, number of observations; m, median of the distribution. Significant differences between GAL1-MAD2 and GAL1-MAD2 cdh1Δ cells were evaluated with a two-sample t test with unequal variances or Wilcoxon rank sum test (significance level: 0.05), respectively, according to the normality or not of the distributions. (B) Proliferation of GAL1-MAD2 (yAC3883) and GAL1-MAD2 cdh1Δ (yAC3885) cells carrying Htb2-mCherry and Clb2-GFP was monitored in microfluidic chamber, in the continuous presence of YEPR medium (i.e., without Mad2 overexpression). Clb2 trajectories were synchronized in silico at the beginning of Clb2 degradation. Individual traces of Clb2 are reported as thin lines, their mean trajectory as thick lines. N, number of trajectories. (C) Duration of anaphase-to-G1 of GAL1-MAD2 and GAL1-MAD2 cdh1Δ cells during the first mitotic arrest. Nuclear segregation was the readout of anaphase onset. N, number of observations; m, median of the distribution. Significant differences between GAL1-MAD2 and GAL1-MAD2 cdh1Δ cells were evaluated with a two-sample t test with unequal variances or Wilcoxon rank sum test (significance level: 0.05), respectively, according to the normality or not of the distributions.

  • Figure S4.
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    Figure S4. related with Fig 3—Size-related features of SAC-active cells.

    (A) Probability density of the cellular size at anaphase onset for gen0 unperturbed, unperturbed, gen0 SAC-active, and SAC-active cells under the two experimental conditions. Sample sizes for GAL1-MAD2: 50 for gen0 unperturbed, 65 for unperturbed, 50 for gen0 SAC-active, and 48 for SAC-active. Sample sizes for tub2-401: 66 for gen0 unperturbed, 71 for unperturbed, 96 for gen0 SAC-active, and 65 for SAC-active. (B) Scatter plot of cellular size at prometaphase versus size at the anaphase onset for unperturbed and SAC-active cells. Linear dependency was tested by evaluation of the Spearman correlation coefficient (r; significance level 0.05) and the slope of the linear regression (slope). Number of points for GAL1-MAD2: 65 for unperturbed, 48 for SAC-active. Number of points for tub2-401: 71 for unperturbed, 65 for SAC-active. (C) Scatter plot of mitotic length versus cellular size at prometaphase for unperturbed and SAC-active cells. Linear dependency was tested by performing a linear regression on data, evaluating the slope λ (significance level: 0.05). Number of points for GAL1-MAD2: 65 for unperturbed, 48 for SAC-active. Number of points for tub2-401: 71 for unperturbed, 65 for SAC-active. (D–F) Description of the filtering and smoothing procedure for size trajectories of gen0 unperturbed, unperturbed, gen0 SAC-active, and SAC-active cells—see the Material and Methods section for details. (D) For each size trajectory, the local size variation ΔA = Ai+1 − Ai was plotted as a function of the size Ai for GAL1-MAD2 (on the left) and tub2-401 (on the right). Yellow dots correspond to high density regions, whereas blue ones to low density regions. Point cloud data were then divided in three clusters (from 0 to 40 μm2, from 40 to 80 μm2, and from 80 to 120 μm2). For each cluster, outlier data (in the white regions) were discriminated from good data (in the green region) according to the distribution of local size variations. Number of points: 2,996 for GAL1-MAD2 and 5,652 for tub2-401. (E) An example of size trajectory adjustment. Raw data are represented by gray dots. From the thresholds that were identified in (D), outliers were detected in the original size trajectories (red points falling on the white regions). Each outlier was replaced by the mean of the two adjacent size values in the trajectory (green point). (F) An example of size trajectory smoothing. Data are represented by blueberry dots. Once filtered, size trajectories were smoothed with a moving average filter (green trajectory).

  • Figure 3.
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    Figure 3. SAC-active cells are larger than unperturbed cells and compensate for size.

    (A) Cell sizes monitored in the experiment. Size of gen0 unperturbed and gen0 SAC-active cells was monitored from the G1 release (Aα) to Clb2 degradation (i.e., anaphase onset, AANA). Size of unperturbed and SAC-active cells was measured from budding (ABUD) to AANA. Dashed lines indicate time intervals in which cell size was not monitored. Size when Clb2 starts to accumulate (i.e., prometaphase, APM) was also monitored. (B) Scatter plot of mitotic size multiplicative increase GMITOSIS (see panel A) versus cellular size at prometaphase in unperturbed and SAC-active cells (log–log). This “size-growth” plot has a slope in the presence of size control and is flat otherwise. Linear dependency was tested by performing a linear regression on data, evaluating the slope λ (significance level: 0.05). Number of points for GAL1-MAD2: 65 for unperturbed, 48 for SAC-active. Number of points for tub2-401: 71 for unperturbed, 65 for SAC-active. (C) Cell size trajectories: filtered and smoothed traces are reported as thin lines and their mean as a thick line. Number of trajectories for GAL1-MAD2: 54 gen0 unperturbed, 65 unperturbed, 45 gen0 SAC-active, 37 SAC-active; number of trajectories for tub2-401: 72 gen0 unperturbed, 75 unperturbed, 78 gen0 SAC-active, 46 SAC-active. (D) Left: simulation of multiple cycles for an individual cell using combined exponential and linear growth. At time = 0, the distribution from which the cell cycle durations are drawn changes from unperturbed to SAC active. Right: all cycles of the simulation are arranged on one growth curve (dashed line). Inset: an example of a cell division in the plot.

  • Figure S5.
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    Figure S5. related with Fig 3—Size-related measurements.

    (A) Saturation of cell growth in gen0 SAC-active and SAC-active cells occurs during mitosis. Local growth rate (dA/dt|A) in function of Clb2 mean levels. Individual measurements (dots) were binned by Clb2 levels and the mean value of each bin (squares) and their trend (thick line) were evaluated. Number of points for GAL1-MAD2: 778 for gen0 unperturbed, 297 for unperturbed, 1,640 for gen0 SAC-active, and 492 for SAC-active; number of points for tub2-401: 781 for gen0 unperturbed, 538 for unperturbed, 3,169 for gen0 SAC-active, and 1,444 for SAC-active. See the Material and Methods section for details about local growth rate measurements. (B) Local growth rate (dA/dt|A) as a function of cell size. Individual measurements (dots) were binned by cell size and the mean value of each bin (squares) and their trend (thick line) were evaluated. Number of points for GAL1-MAD2: 778 for gen0 unperturbed, 297 for unperturbed, 1,640 for gen0 SAC-active, and 492 for SAC-active cells. Number of points for tub2-401: 781 for gen0 unperturbed, 538 for unperturbed, 3,169 for gen0 SAC-active, and 1,444 for SAC-active. See the Material and Methods section for details about local growth rate measurements. (C) Examples of morphologies of gen0 unperturbed, gen1 unperturbed, gen0 SAC-active, and gen1 SAC-active cells under the two experimental conditions. Scale bar: 5 μm. (D) Evaluation of cell size at the cell cycle entry as a function of the cycle number from checkpoint activation, assuming two alternative models of cell growth: exponential growth or exponential with linear growth (used in the simulations).

  • Figure S6.
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    Figure S6. related to Fig 4—Mass-spec analysis, PCA, and GO categories.

    (A) Expression of the CDC20-127 allele bypasses the mitotic arrest induced by Mad2 overexpression. GAL1-MAD2 (yAC2465), GAL1-MAD2 mad3Δ (yAC436), and GAL1-MAD2 tetO2-CDC20-127 (yAC2807) cells were synchronized in G1 with α-factor and released in the presence of galactose to induce Mad2 overexpression. Two populations of yAC2807 were monitored: one expressing and one not expressing CDC20-127 (gen0 unperturbed and gen0 SAC-active, respectively). α-factor was re-added after 1h30 min from the release and then every 2 h, to re-synchronize cells in the subsequent G1 phase. Cells were monitored for 7 h and sampled for FACS analysis to measure DNA content. The leakage from the promoter is minimal, as can be observed comparing the first round of adaptation in cells expressing or not CDC20-127 (compare GAL1-MAD2 and gen0 SAC-active cells). (B) PCA of label-free quantities (LFQ) intensities for all samples used in the proteomic analysis after batch correction. (C, D) Scatter plot of P-values of GO enrichment for down-regulated and up-regulated proteins ranked by positive log2-fold change. GO terms outside a circle with radius three are highlighted in red and reported in the figure legend.

  • Figure 4.
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    Figure 4. The proteome of SAC-active cells undergoes global changes, which overlap with the ESR.

    (A) Scatter plot of log2-fold changes showing the common expression pattern of GAL1-MAD2 and tub2-401. Proteins expressed at a log2-fold change above 0.5 are highlighted. Pearson correlation is calculated for all proteins and the highlighted subset, respectively. (B) Same as (A), highlighting proteins that are related to the ESR. Pearson correlation is separately calculated for proteins induced in, repressed in, and unrelated to the ESR, respectively. (C) Heatmap showing hierarchical clustering of protein expression in SAC-active cells and gene expression in other yeast strains: (i) early and late time points of cells upon benomyl treatment (31); (ii) the APC/C mutant cdc23-1; (iii) a mutant of CDK1, cdc28-4, with low activity in the S- and M-phase (32); (iv) a set of aneuploid cells (A2, A3, A9, A10, A13, A14, and A15) (33); (v) cells in stationary phase which show a very strong ESR expression profile (YPD 6 h) (29); (vi) data that do not show an ESR (cdc15-2 cells (32)) and (vii) data which show an expression profile opposite to ESR (cells grown at low temperature (29)). The column to the left shows the normalized stress response intensity (SRI) that quantifies the presence of an ESR response in a sample—see the Materials and Methods section and Table S1 for details.

  • Figure 5.
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    Figure 5. Cell size and proliferative status of SAC-active cells are reversible.

    (A) Left: simulation of the withdrawal experiment. At time = 0 the distribution from which the cell cycle durations are drawn changes from SAC active to unperturbed. Right: Histograms of the size at entry (i.e., right after division) of the first five cycles after withdrawal. Each histogram corresponds to 200 individual simulations. (B) Experimental setup of the withdrawal experiment. tub2-401 cells (yAC4096) grew in three different conditions: unperturbed at 30°C, SAC-active at 22°C, and withdraw were shifted to 30°C after 20 h at 22°C. Cells were monitored every hour for 9 h after the temperature shift. (C) Cell size distributions of unperturbed and cells after withdraw, measured at 0 h, 3 h, and 9 h after the temperature shift. (D) Overlap of cell size distribution after withdraw compared with unperturbed and SAC-active cells during the entire experiment—see the Material and Methods section for details. On the left: evaluation of convergence to unperturbed distribution at 9 h; on the right: evaluation of divergence from SAC-active distribution at 0 h. Individual dots represent biological replicates, whereas continuous lines the mean behaviors. (E) Growth curves of unperturbed, SAC-active, and withdrawn cells. Individual dots represent biological replicates, whereas continuous lines the mean behaviors.

  • Figure 6.
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    Figure 6. Cellular responses supporting proliferation in the presence of an active mitotic checkpoint.

    Schematic of the behavior of SAC-active cells. Under constant checkpoint activity, SAC-active cells are exposed to several risks and stressful conditions, to which they respond with appropriate strategies.

Supplementary Materials

  • Figures
  • Table S1 Values of normalized Stress Response Intensity of Fig 4C.

  • Table S2 Yeast strains.

  • Table S3 Plasmids.

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Proliferation with an active checkpoint
Andrea Corno, Elena Chiroli, Fridolin Gross, Claudio Vernieri, Vittoria Matafora, Stefano Maffini, Marco Cosentino Lagomarsino, Angela Bachi, Andrea Ciliberto
Life Science Alliance May 2019, 2 (3) e201900380; DOI: 10.26508/lsa.201900380

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Proliferation with an active checkpoint
Andrea Corno, Elena Chiroli, Fridolin Gross, Claudio Vernieri, Vittoria Matafora, Stefano Maffini, Marco Cosentino Lagomarsino, Angela Bachi, Andrea Ciliberto
Life Science Alliance May 2019, 2 (3) e201900380; DOI: 10.26508/lsa.201900380
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