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RNA stores tau reversibly in complex coacervates

Zhang, Xuemei, Lin, Yanxian, Eschmann, Neil A., Zhou, Hongjun, Rauch, Jennifer N., Hernandez, Israel, Guzman, Elmer, Kosik, Kenneth S., Han, Songi·2017·PLOS Biology
DOI 10.1371/journal.pbio.2002183PMC PMC5500003

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Fig 1 Tau PhotoActivatable Ribonucleoside-enhanced Individual-nucleotide resolution UV Cross-Linking ImmunoPrecipitation and high-throughput sequencing (PAR-iCLIP) in tau-expressing human embryonic kidney cells (HEK) and human-induced pluripotent stem cell (hiPSC) -derived neurons. Phosphor images in the blue frames (A-C) show 32P-labelled RNA crosslinked to tau protein in HEK cells expressing tau (A-B) and in hiPSC-derived neurons with endogenous tau (C). PAR-iCLIP in HEK cells expressing wild-type tau (A, lane 2) or tau P301L-CFP (B, lane 2; nota bene: the fused cyan fluorescent protein [CFP] retards the migration of tau). (C) PAR-iCLIP of endogenous wild-type tau in hiPSC-derived neurons (C, lane 2). The antibodies anti-tau HJ 8.5, anti-green fluorescence protein (GFP) and anti- Cyclin–dependent kinase 5 (CDK5) were used for protein precipitation. No RNase was added, unless specified. PAR-iCLIP with GFP as a control (A-B, lane 1), with CDK5 as a control (C, lane 3) and no UV control (C, lane 1). A small RNA signal was visible in the absence of cross-linking (no UV control) in hiPSC-derived neurons (C, lane 1), suggesting a small portion of RNA may associate with tau in vitro after cell lysis. The RNA-protein complexes from Cross-Linking ImmunoPrecipitation (CLIP) marked by rectangles were cut from the blot for DNA library preparation. Note that 2 regions of GFP and CDK5 were cut out as sequencing controls in which the lower molecular weight (MW) band corresponds to GFP or CDK5. (D-E) Percentage of tau-CLIP reads that are mapped to 8 human genome regions in HEK cells (D) and hiPSC-derived neurons (E). (F-G) Enrichment of tRNA in tau-CLIP of HEK cells (F) and hiPSC-derived neurons (G) as discussed in text. The numerical data used in (D-G) are included in S1 Data.
Fig 1 Tau PhotoActivatable Ribonucleoside-enhanced Individual-nucleotide resolution UV Cross-Linking ImmunoPrecipitation and high-throughput sequencing (PAR-iCLIP) in tau-expressing human embryonic kidney cells (HEK) and human-induced pluripotent stem cell (hiPSC) -derived neurons. Phosphor images in the blue frames (A-C) show 32P-labelled RNA crosslinked to tau protein in HEK cells expressing tau (A-B) and in hiPSC-derived neurons with endogenous tau (C). PAR-iCLIP in HEK cells expressing wild-type tau (A, lane 2) or tau P301L-CFP (B, lane 2; nota bene: the fused cyan fluorescent protein [CFP] retards the migration of tau). (C) PAR-iCLIP of endogenous wild-type tau in hiPSC-derived neurons (C, lane 2). The antibodies anti-tau HJ 8.5, anti-green fluorescence protein (GFP) and anti- Cyclin–dependent kinase 5 (CDK5) were used for protein precipitation. No RNase was added, unless specified. PAR-iCLIP with GFP as a control (A-B, lane 1), with CDK5 as a control (C, lane 3) and no UV control (C, lane 1). A small RNA signal was visible in the absence of cross-linking (no UV control) in hiPSC-derived neurons (C, lane 1), suggesting a small portion of RNA may associate with tau in vitro after cell lysis. The RNA-protein complexes from Cross-Linking ImmunoPrecipitation (CLIP) marked by rectangles were cut from the blot for DNA library preparation. Note that 2 regions of GFP and CDK5 were cut out as sequencing controls in which the lower molecular weight (MW) band corresponds to GFP or CDK5. (D-E) Percentage of tau-CLIP reads that are mapped to 8 human genome regions in HEK cells (D) and hiPSC-derived neurons (E). (F-G) Enrichment of tRNA in tau-CLIP of HEK cells (F) and hiPSC-derived neurons (G) as discussed in text. The numerical data used in (D-G) are included in S1 Data.CC BY · PubMed Central
Fig 2 Enrichment of tRNA in PhotoActivatable Ribonucleoside-enhanced Individual-nucleotide resolution UV Cross-Linking ImmunoPrecipitation and high-throughput sequencing (PAR-iCLIP) data. (A) Cross-Linking ImmunoPrecipitation (CLIP) cDNA reads from tau expressed in human-induced pluripotent stem cell (hiPSC)-derived neurons (neuron CLIP) and from tau expressed in human embryonic kidney (HEK) cells (HEK cell CLIP) that aligned to the chr15.tRNA4-ArgTCG tRNA were found in all CLIP samples, and demonstrated a similar pattern of crosslinking. (B) Analysis of cross-linked sites along tRNA secondary structure demonstrates the anticodon preference, in which the anticodon (colored red) region is designated as position 1–3 for alignment purpose. The colored illustration of tRNA secondary structure is displayed as an inset, and below the x axis in one dimension. The numerical data used in (B) are included in S1 Data.
Fig 2 Enrichment of tRNA in PhotoActivatable Ribonucleoside-enhanced Individual-nucleotide resolution UV Cross-Linking ImmunoPrecipitation and high-throughput sequencing (PAR-iCLIP) data. (A) Cross-Linking ImmunoPrecipitation (CLIP) cDNA reads from tau expressed in human-induced pluripotent stem cell (hiPSC)-derived neurons (neuron CLIP) and from tau expressed in human embryonic kidney (HEK) cells (HEK cell CLIP) that aligned to the chr15.tRNA4-ArgTCG tRNA were found in all CLIP samples, and demonstrated a similar pattern of crosslinking. (B) Analysis of cross-linked sites along tRNA secondary structure demonstrates the anticodon preference, in which the anticodon (colored red) region is designated as position 1–3 for alignment purpose. The colored illustration of tRNA secondary structure is displayed as an inset, and below the x axis in one dimension. The numerical data used in (B) are included in S1 Data.CC BY · PubMed Central
Fig 3 Tau tRNA binding by gel shift assay and isothermal titration calorimetry (ITC). (A) Direct titration experiment shows 4R2N tau induces a mobility shift in tRNALys. To determine the Kd value, direct titration experiment was done, which requires trace RNA concentrations to meet the assumption used in the equation that derives the Kd value. The assumption is that the total protein concentration is approximately the free protein concentration at equilibrium, and that protein binding to RNA is negligible. In the direct titration experiments 26 nM, tRNA was used and protein concentration spans from 20 nM to 2 μM. (B) The fraction of bound tRNA by 4R2N tau plotted as a function of the monomeric tau concentration and fit to the Hill equation, y = 1 / [1 + (Kd / x)n]. (C) Yeast tRNA was titrated into solutions of 4R2N tau in an ITC experiment. The top panel shows the raw incremental-titration. The area under each peak is integrated and plotted against the tRNA:tau molar ratio and fitted to an independent binding model (the bottom panel), as discussed in Materials and methods. (B-C) SEM is reported from n = 3. (D) The stoichiometric binding experiments were performed by varying the tau:RNA molar ratio at a constant 2.6 μM concentration of tRNA, which approximates the saturation concentration (more than 5 times the Kd of 460 nM). The representative data of 3 independent experiments are shown. (E) Fraction of bound tRNA from the different bands in (D) is plotted over the molar tau:tRNA ratio. (F) Fraction of bound tau plotted as a function of tau:tRNA molar ratios and compared to the theoretical saturation binding curves (dotted lines) with protein:RNA molar stoichiometries of 1:1 to 6:1. The theoretical curves serve the purpose showing that multiple tau molecules bind tRNA with increasing tau concentrations, while the model is not meant to fit the data, given that multiple populations with different tau:tRNA ratios will coexist. The numerical data used in (B), (C), (E), and (F) are included in S1 Data.
Fig 3 Tau tRNA binding by gel shift assay and isothermal titration calorimetry (ITC). (A) Direct titration experiment shows 4R2N tau induces a mobility shift in tRNALys. To determine the Kd value, direct titration experiment was done, which requires trace RNA concentrations to meet the assumption used in the equation that derives the Kd value. The assumption is that the total protein concentration is approximately the free protein concentration at equilibrium, and that protein binding to RNA is negligible. In the direct titration experiments 26 nM, tRNA was used and protein concentration spans from 20 nM to 2 μM. (B) The fraction of bound tRNA by 4R2N tau plotted as a function of the monomeric tau concentration and fit to the Hill equation, y = 1 / [1 + (Kd / x)n]. (C) Yeast tRNA was titrated into solutions of 4R2N tau in an ITC experiment. The top panel shows the raw incremental-titration. The area under each peak is integrated and plotted against the tRNA:tau molar ratio and fitted to an independent binding model (the bottom panel), as discussed in Materials and methods. (B-C) SEM is reported from n = 3. (D) The stoichiometric binding experiments were performed by varying the tau:RNA molar ratio at a constant 2.6 μM concentration of tRNA, which approximates the saturation concentration (more than 5 times the Kd of 460 nM). The representative data of 3 independent experiments are shown. (E) Fraction of bound tRNA from the different bands in (D) is plotted over the molar tau:tRNA ratio. (F) Fraction of bound tau plotted as a function of tau:tRNA molar ratios and compared to the theoretical saturation binding curves (dotted lines) with protein:RNA molar stoichiometries of 1:1 to 6:1. The theoretical curves serve the purpose showing that multiple tau molecules bind tRNA with increasing tau concentrations, while the model is not meant to fit the data, given that multiple populations with different tau:tRNA ratios will coexist. The numerical data used in (B), (C), (E), and (F) are included in S1 Data.CC BY · PubMed Central
Fig 4 Tau and RNA forms droplet in vitro. (A) Bright field snapshots of droplets from 400 μM Δtau187 and 800 μg/ml poly(A) showing 2 droplets seamlessly fusing (highlighted with red circle). (B) Confocal microscopy image of Δtau187 labeled with Alexa-488 of the droplets from the same sample as in (A). 50 μM Alexa-488 labeled Δtau187 mixed with 350 μM MTSL labeled Δtau187 of droplets formed immediately after adding 800 μg/ml poly(A) RNA. Both (A) and (B) were sampled at room temperature and without added NaCl.
Fig 4 Tau and RNA forms droplet in vitro. (A) Bright field snapshots of droplets from 400 μM Δtau187 and 800 μg/ml poly(A) showing 2 droplets seamlessly fusing (highlighted with red circle). (B) Confocal microscopy image of Δtau187 labeled with Alexa-488 of the droplets from the same sample as in (A). 50 μM Alexa-488 labeled Δtau187 mixed with 350 μM MTSL labeled Δtau187 of droplets formed immediately after adding 800 μg/ml poly(A) RNA. Both (A) and (B) were sampled at room temperature and without added NaCl.CC BY · PubMed Central
Fig 5 Tau-RNA droplets form a complex coacervate phase. (A) Representative bright-field images of tau-tRNA droplet samples at room temperature with varying [NaCl]. (B) Droplet coverage (in %) with poly(A) or tRNA in room temperature with varying [NaCl]. Δtau187:RNA in (A) and (B) were maintained at a mass ratio of 7:1 (corresponding to a charge ratio of 1.2:1) and a total mass concentration of 2 mg/ml. (C) Droplet coverage with poly(A) or tRNA with varying Δtau187: RNA charge ratios. The total mass concentrations are indicated in the legends. Samples made by mixing of 80 μM Δtau187 with 222 μg/ml poly(A)/tRNA or 161 μM Δtau187 with 444 μg/ml tRNA gave the highest droplet coverage (%), which correspond to charge ratio of 1.3–1.2 between tau and RNA. Error bars in (B) and (C) represent the standard deviation from n = 3. (D) Representative bright-field images of tau-RNA droplets as a function of incubation temperature. To record these images, the temperature was ramped from 19ºC to 25°C at 1°C per minute to acquire confocal images with bright field illumination. The samples for these images are generated from 100 μM tau mixed with poly(U) at approximately 1:1 charge ratio in the presence of 30 mM NaCl. (E) Representative bright-field images of tau-RNA droplet samples incubated at 37°C under otherwise different sample conditions. The concentration for tau, poly(U) RNA and NaCl are (i) 5 μM, 15 μg/ml, 0 mM; (ii) 5 μM, 15 μg/ml, 100 mM; (iii) 2.5 μM, 7.5 μg/ml, 100 mM; (iv) 1 μM, 3 μg/ml, 100 mM. Arrows highlight some of the droplets in images (ii) and (iii). Through Fig 5, scale bars are for 50 μm and all samples were prepared with Δtau187/322C in 20 mM ammonium acetate at pH 7.0. The numerical data used in (B) and (C) are included in S1 Data.
Fig 5 Tau-RNA droplets form a complex coacervate phase. (A) Representative bright-field images of tau-tRNA droplet samples at room temperature with varying [NaCl]. (B) Droplet coverage (in %) with poly(A) or tRNA in room temperature with varying [NaCl]. Δtau187:RNA in (A) and (B) were maintained at a mass ratio of 7:1 (corresponding to a charge ratio of 1.2:1) and a total mass concentration of 2 mg/ml. (C) Droplet coverage with poly(A) or tRNA with varying Δtau187: RNA charge ratios. The total mass concentrations are indicated in the legends. Samples made by mixing of 80 μM Δtau187 with 222 μg/ml poly(A)/tRNA or 161 μM Δtau187 with 444 μg/ml tRNA gave the highest droplet coverage (%), which correspond to charge ratio of 1.3–1.2 between tau and RNA. Error bars in (B) and (C) represent the standard deviation from n = 3. (D) Representative bright-field images of tau-RNA droplets as a function of incubation temperature. To record these images, the temperature was ramped from 19ºC to 25°C at 1°C per minute to acquire confocal images with bright field illumination. The samples for these images are generated from 100 μM tau mixed with poly(U) at approximately 1:1 charge ratio in the presence of 30 mM NaCl. (E) Representative bright-field images of tau-RNA droplet samples incubated at 37°C under otherwise different sample conditions. The concentration for tau, poly(U) RNA and NaCl are (i) 5 μM, 15 μg/ml, 0 mM; (ii) 5 μM, 15 μg/ml, 100 mM; (iii) 2.5 μM, 7.5 μg/ml, 100 mM; (iv) 1 μM, 3 μg/ml, 100 mM. Arrows highlight some of the droplets in images (ii) and (iii). Through Fig 5, scale bars are for 50 μm and all samples were prepared with Δtau187/322C in 20 mM ammonium acetate at pH 7.0. The numerical data used in (B) and (C) are included in S1 Data.CC BY · PubMed Central
Fig 6 Tau in condensed droplets assumes solution state properties. (A-C) Continuous wave electron paramagnetic resonance (cw EPR) spectra obtained at room temperature of 500 μM Δtau187-SL in droplets formed with 1.5 mg/ml poly(A) RNA (blue in A) and 1.5 mg/ml tRNA (green in B) is unaltered from solution before adding RNA (red in A and B). Cw EPR line shape upon adding 125 μM heparin (black in C) show dramatic line broadening (compared to red in C). Double electron-electron resonance (DEER) of Δtau187-SL2 in droplets formed with 1.5 mg/ml poly(A) RNA (blue in D) and 1.5 mg/ml tRNA (green in E), as well as upon incubation with 137.5 μM heparin (black in F) compared to Δtau187-SL2 in solution (red in D-F). The numerical data are included in S1 Data.
Fig 6 Tau in condensed droplets assumes solution state properties. (A-C) Continuous wave electron paramagnetic resonance (cw EPR) spectra obtained at room temperature of 500 μM Δtau187-SL in droplets formed with 1.5 mg/ml poly(A) RNA (blue in A) and 1.5 mg/ml tRNA (green in B) is unaltered from solution before adding RNA (red in A and B). Cw EPR line shape upon adding 125 μM heparin (black in C) show dramatic line broadening (compared to red in C). Double electron-electron resonance (DEER) of Δtau187-SL2 in droplets formed with 1.5 mg/ml poly(A) RNA (blue in D) and 1.5 mg/ml tRNA (green in E), as well as upon incubation with 137.5 μM heparin (black in F) compared to Δtau187-SL2 in solution (red in D-F). The numerical data are included in S1 Data.CC BY · PubMed Central
Fig 7 tRNA transfection accumulates sarkosyl insoluble tau in human-induced pluripotent stem cell (hiPSC) derived neurons. (A) Representative western blot of neurons harboring a P301L tau mutation transfected with tRNA, but not cells transfected in the absence of nucleic acids (Mock) present evidence for accumulation of sarkosyl insoluble tau (Ins.) as seen in the intense band in lane 9 labeled with PHF-1 antibody. Addition of tRNA to the lysis buffer is insufficient to increase the tau present in the insoluble fractions (compare Mock + tRNA, lane 6 to tRNA, lane 9). (B-C) Quantification of PHF-1 tau and β-actin level for both neurons harboring a P301L tau mutation (B) and neurons expressing wild type tau (C) are shown. Error bar represents standard error of the mean. * p < 0.05, *** p < 0.001, n > 3. The numerical data used in B and C are included in S1 Data.
Fig 7 tRNA transfection accumulates sarkosyl insoluble tau in human-induced pluripotent stem cell (hiPSC) derived neurons. (A) Representative western blot of neurons harboring a P301L tau mutation transfected with tRNA, but not cells transfected in the absence of nucleic acids (Mock) present evidence for accumulation of sarkosyl insoluble tau (Ins.) as seen in the intense band in lane 9 labeled with PHF-1 antibody. Addition of tRNA to the lysis buffer is insufficient to increase the tau present in the insoluble fractions (compare Mock + tRNA, lane 6 to tRNA, lane 9). (B-C) Quantification of PHF-1 tau and β-actin level for both neurons harboring a P301L tau mutation (B) and neurons expressing wild type tau (C) are shown. Error bar represents standard error of the mean. * p < 0.05, *** p < 0.001, n > 3. The numerical data used in B and C are included in S1 Data.CC BY · PubMed Central

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Metadata

Authors
Zhang, X., Lin, Y., Eschmann, N. A., Zhou, H., Rauch, J. N., Hernandez, I., Guzman, E., Kosik, K. S., & Han, S.
Venue
PLOS Biology
Publisher
Public Library of Science (PLoS)
Published
2017-07-06
Volume
15
Issue
7
Pages
e2002183
ISSN
1545-7885
DOI
10.1371/journal.pbio.2002183
PMC
PMC5500003
Cited by
302
References
11
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.