Abstract
Ribosome biogenesis is among the most resource-intensive cellular processes, with ribosomal proteins accounting for up to half of all newly synthesized proteins in eukaryotic cells. During stress, cells shut down ribosome biogenesis in part by halting rRNA synthesis, potentially leading to massive accumulation of aggregation-prone ‘orphan’ ribosomal proteins (oRPs). Here we show that, during heat shock in yeast and human cells, oRPs accumulate as reversible peri-nucleolar condensates recognized by the Hsp70 co-chaperone Sis1/DnaJB6. oRP condensates are liquid-like in cell-free lysate but solidify upon depletion of Sis1 or inhibition of Hsp70. When cells recover from heat shock, oRP condensates disperse in a Sis1- and Hsp70-dependent manner, and the oRP constituents are incorporated into functional ribosomes in the cytosol, enabling cells to efficiently resume growth. Preserving biomolecules in reversible condensates—like mRNAs in cytosolic stress granules and oRPs at the nucleolar periphery—may be a primary function of the Hsp70 chaperone system.
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Data availability
The MS proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD039068 and PXD039134. RNA-seq raw sequence files and processed data were deposited in the Gene Expression Omnibus (accession no. GSE237174). Source data are provided with this paper. Any other potential type of data used to interpret the finding can be provided upon request to corresponding author.
Code availability
Custom code used for the image analysis are deposited at Zenodo (https://doi.org/10.5281/zenodo.8076227).
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Acknowledgements
We are grateful to H. An and W. Harper for sharing the HCT116 RPL26–HaloTag cell line. We thank V. Bindokas and C. Labno at the University of Chicago Integrated Light Microscopy Core (RRID: SCR_019197) for imaging assistance. We are especially grateful to B. Glick and lab members for the yeast HaloTag construct and advice on using JF dyes in yeast. We thank S. Kron for use of gel imaging instruments, and K. Lin for assistance aligning the Squires Lab custom wide-field setup and camera calibration. We also thank members of the Pincus, Squires and Drummond labs for helpful discussions. J.A.M.B. acknowledges fellowship support from the Helen Hay Whitney Foundation. This work was supported by NIH grants R01 GM138689 to D.P., R35 GM144278 to D.A.D., support from the Neubauer Family Foundation to A.H.S., and NSF QLCI QuBBE grant OMA-2121044 to D.P. and A.H.S.
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Conceptualization: A.A. and D.P.; methodology: A.A., R.G., O.C.S., J.A.M.B., K.H., S.K.K. and A.H.S.; formal analysis: A.A., O.C.S., K.H., A.H.S. and D.P.; investigation: A.A., R.G., O.C.S., J.A.M.B., S.K.K., K.A.D., S.L.-W. and M.G.I.; resources: A.A., J.A.M.B., D.A.D., A.H.S. and D.P.; writing—original draft: A.A. and D.P.; writing—review and editing: all authors; visualization: A.A., O.C.S., K.H. and D.P.; supervision: D.A.D., A.H.S. and D.P.; funding acquisition: D.A.D., A.H.S. and D.P.
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Extended data
Extended Data Fig. 1 Sis1 localization and interactions during heat shock.
(a) Left: Schematic of how to bisect the nucleus with the nucleolus on one side by finding the line angle with the maximum difference in signal of the nucleolar marker in the two halves. Middle: Representative 2D projections of cells showing Nsr1 (blue) to mark the nucleolus and Sis1 (green). Line is set to maximize the difference in nucleolar signal and the ratio of Sis1 in the two halves is calculated. Right: Sis1 ratio as a function of the line angle rotated as depicted in the schematic to the left. (b) Quantification of Sis1 cytosolic foci per cell in the conditions listed. Foci were identified using the FindFoci plugin in ImageJ. Statistical significance was determined by Brown-Forsythe and Welch one-way ANOVA test followed by Games-Howell multiple comparison tests. n obtained from 3 independent experiment. (c) Volcano plot of Sis1-APEX2 interactors during heat shock. (d) Scatter plot showing the percentage of disorder in Sis1 interactors relative the whole proteome. P values were calculated with unpaired two-tailed Welch’s t-test. n = 2 biological replicates. Each dot symbolizes individual proteins, with ‘n’ representing 5151 proteins for the entire yeast proteome and 731 proteins for the Sis1 interactors induced by heat shock. Data is representative of 2 biologically independent experiments. (e) Bar plots representing the amino acid sequences enrichment of the Sis1 interactors compared to the yeast proteome. Data is representative of 2 biologically independent experiments. (f) Biological replicates of Sis1-3xFlag IP interactors.
Extended Data Fig. 2 Interaction and localization of pulse-labeled ribosomal proteins with Sis1.
(a) IP of Sis1-3xFlag and either mature or new Rpl25-Halo and Rps9a-Halo from cells left unstressed or heat shocked at 39 °C for the indicated times. n = 2 biologically independent experiment. (b) In the absence of heat shock, pulse-labeled RPs localize immediately to the cytosol. Micrograph represents data obtained from 3 biologically independent experiments. (c) Left Panel: Lattice light sheet live imaging of yeast under heat shock (39 °C, 10 min) expressing Sis1-mVenus and labeled for either new or mature Rpl25-Halo. Right Panel: Dot plot representing the colocalization coefficient (Mander’s overlap coefficient) of Sis1-mVenus with either mature or new Rpl25-Halo in heat shocked cells (39 °C, 10 min). n = number of cells pooled from 3 biologically independent replicates. (d) As in (c) but for Rps9a-Halo. n = number of cells pooled from 3 biologically independent replicates. (e) As in (c) but for the late joining subunit Rpl29-Halo. n = number of cells pooled from 3 biologically independent replicates. (f) As in (c) but for the late joining subunit Rps3-Halo. n = number of cells pooled from 3 biologically independent replicates. P values were calculated with unpaired two-tailed Welch’s t-test.
Extended Data Fig. 3 Localization of pre-60S ribosome biogenesis factors during heat shock.
(a) Illustrate showing the association of assembly factors with various states of pre60S maturation. Clustering and coloration in the diagram indicate the time points of stable association and dissociation from the maturing particle, as denoted by the horizontal lines. (b-p) LLS imaging of Live cells representing the localization of oRpl26a during heat shock in context of pre-60S ribosome assembly factors as depicted in (a). Scale bar = 2 µm. Inset shows the normalized line scan graph of representing assembly factors across the oRpl26a signal.
Extended Data Fig. 4 Cell biological and transcriptional effects of Ifh1 depletion during heat shock.
(a) Immunoblot showing of the level of Ifh1-mAID-3xFlag upon incubation with 5ph-IAA and β-estradiol. PGK1 level is used as loading control between the samples. (b) HSE-YFP reporter heat shock time course showing reduced HSR induction when Ifh1 is depleted. Data are presented as mean ± S.D. n = 3 biologically independent sample. (c) RT-qPCR of the HSR target gene transcript SSA4 over a heat shock time course in the absence and presence of Ifh1 depletion. Data are presented as mean ± S.D n = 3 biologically independent sample. (d) LLS live-imaging of yeast cells with endogenously tagged Sis1-mVenus (green), Hsp104-TFP (blue), Sec61-Halo (red) and Nsr1-mScarlet-I (white) under non-stress (30 °C) and heat shock (39 °C, 10 min) in the absence and presence of Ifh1 depletion. (e) Quantification of Sis1 cytosolic foci per cell in the conditions shown in (d). Statistical significance was assessed using the Brown-Forsythe and Welch ANOVA test, along with Games-Howell multiple post hoc comparisons. n denotes number of cells from 3 independent experiment.
Extended Data Fig. 5 oRP condensates are stable and heat shock-dependent.
(a) oRP proteins are stable (not degraded) in condensates in cells. (b) oRP condensates are more abundant in lysate from heat-shocked cells. Micrograph represents data of 3 biologically independent experiments.
Extended Data Fig. 6 Temperature scan and RNA assessment of oRP condensates.
(a) Illustrate depicting the workflow to label newly synthesized RP in yeast and lysate preparation to conduct temperature scan. (b) Micrograph of oRP condensate prepared from non-stressed or heat shocked yeast and upon incubation at indicated temperature. n = 3 biologically independent experiments. (c) RNA dye (SYTO RNASelect, 0.5 mM, 10 min) is excluded from the oRP condensate. n = 3 biologically independent experiments. (d) oRP condensates are resistant to RNaseIf (5units/µl, 15 min, 25 °C). (e) Quantification of number of droplets per field in buffer or RNaseIf treatment to the lysate. P values were calculated with unpaired two-tailed Welch’s t-test. n is representing number of droplets quantified in microscopic field of 53 and 42 for Buffer and RNaseI conditions respectively.
Extended Data Fig. 7 Effect of Hsp70 inhibition and hexanediol on oRP condensates in lysate.
(a) Effect of Hsp70 inhibition in the morphology of Rpl26a and Sis1 condensates. (b) Effect of 5% 1,6-HD upon the condensates with or without Hsp70 inhibition. The micrograph represents data derived from 3 independent experiments.
Extended Data Fig. 8 oRPs in condensates are not degraded and are transported to the cytosol upon recovery.
(a) Live cell time lapse imaging of the spatial distribution of Rps4b (magenta) and Sis1-mVenus (green) during sustained heat shock and recovery. (b) Quantification of the fraction of cytosolic Rps4b signal under sustained HS or recovery. Statistical significance was established using the Brown-Forsythe and Welch one-way ANOVA test, followed by Dunnett T3 multiple comparison analyses. n = number of cells pooled from 3 biologically independent replicates. (c) Fraction of total pulse labeled Rpl26a or Rps4b remaining after chase for 15 minutes at indicated temperature. n=number of cells pooled from 3 biologically independent replicates.
Extended Data Fig. 9 oRP condensate reversibility depends upon Sis1 availability.
(a) Imaging of Sis1-mVenus (green) and Nup49-mScarlet-I (red) following Sis1 depletion or not. (b) Quantification of fraction of nuclear Sis1 upon Sis1 depletion or not. P values were calculated with unpaired two-tailed Welch’s t-test. n denotes number of cells as obtained from 4 independent experiment. n = number of cells pooled from 4 biologically independent replicates. (c) LLS imaging of Hsp104-mKate2 during heat shock (39 °C, 15 mins) pre-depleted for Sis1 (green) or not. (d) Quantification of Hsp104-mKate2 foci per cell for (c). P values were calculated with unpaired two-tailed Welch’s t-test. n denotes number of cells from 3 independent experiments. n = number of cells pooled from 3 biologically independent replicates. (e) LLS live cell imaging of Rps4b (magenta) and the nucleolar marker Nsr1 (blue) during heat shock and recovery in the absence or presence of Sis1 depletion. (f) Quantification of the fraction of cytosolic Rps4b under sustained HS or recovery in the absence or presence of Sis1 depletion. P values were calculated with unpaired two-tailed Welch’s t-test. n denotes number of cells obtained from 3 independent experiment. n = number of cells pooled from 3 biologically independent replicates.
Supplementary information
Supplementary Information
Supplementary video and table legends.
Supplementary Video 1
Four-channel 4D lattice light-sheet imaging during heat shock. Yeast expressing Sis1–mVenus (green), Sec61–HaloTag labelled with JF646 (red), Nsr1–mScarlet-I (white) and Hsp104–mTFP (blue) were imaged following heat shock. The video illustrates the dynamic yet consistent buildup of Sis1 at the nucleolar periphery and cytosolic foci, occurring after a 10-min heat shock.
Supplementary Video 2
oRP condensates are stable and dynamic at the nucleolar periphery. Cells expressing Sis1–mVenus (green), Nsr1–mScarlet-I (blue) and Rpl26a–HaloTag (magenta) labelled for new Rpl26a–HaloTag labelled with JF646 and imaged following heat shock.
Supplementary Video 3
Fission and fusion of oRP condensates in lysate. Rpl26a–HaloTag (magenta) pulse labelled with JF646 before heat shock imaged over time in cryo-milled yeast extract. The video depicts the temporal dynamics of fusion and fission events involving newly synthesized Rpl26a.
Supplementary Video 4
Hsp70 co-localizes with Sis1 at the nucleolar periphery during heat shock. Cells expressing HaloTag-Ssa1 labelled with JF646 (red), Sis1–mVenus (green) and Nsr1–mScarlet-I (blue) were imaged following heat shock. The video showcases the dynamic nature and co-localization of Sis1 with Ssa1 after a 10 min heat shock.
Supplementary Tables
Supplementary Table 1. Yeast strains used in this study. Supplementary Table 2. Sis1–APEX2 MS results. Supplementary Table 3. Sis1–3xFlag MS results. P values were calculated with unpaired two-tailed Student’s t-test. Supplementary Table 4. sgRNA and repair template used in this study
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Ali, A., Garde, R., Schaffer, O.C. et al. Adaptive preservation of orphan ribosomal proteins in chaperone-dispersed condensates. Nat Cell Biol 25, 1691–1703 (2023). https://doi.org/10.1038/s41556-023-01253-2
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DOI: https://doi.org/10.1038/s41556-023-01253-2
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