Abstract
Neurons, astrocytes and oligodendrocytes locally regulate protein translation within distal processes. Here, we tested whether there is regulated local translation within peripheral microglial processes (PeMPs) from mouse brain. We show that PeMPs contain ribosomes that engage in de novo protein synthesis, and these are associated with transcripts involved in pathogen defense, motility and phagocytosis. Using a live slice preparation, we further show that acute translation blockade impairs the formation of PeMP phagocytic cups, the localization of lysosomal proteins within them, and phagocytosis of apoptotic cells and pathogen-like particles. Finally, PeMPs severed from their somata exhibit and require de novo local protein synthesis to effectively surround pathogen-like particles. Collectively, these data argue for regulated local translation in PeMPs and indicate a need for new translation to support dynamic microglial functions.
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Data availability
All data are available upon request. Raw and analyzed RNA-seq data are available at the Gene Expression Omnibus under accession no. GSE161460. Additional raw data are available at https://bitbucket.org/jdlabteam/vasek_microglia_local_translation_phagocytosis/src/master/. Source data are provided with this paper.
Code availability
All code is available at https://bitbucket.org/jdlabteam/vasek_microglia_local_translation_phagocytosis/src/master/.
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Acknowledgements
We thank P. Bayguinov, G. Strout and the Washington University Center for Cellular Imaging for their expertise and training in live slice imaging and electron microscopy; K. Sakers for training and support; C. Weichselbaum for comments on the manuscript; and the Genome Technology Access Center (GTAC@MGI) for sequencing and library preparation. Funding was provided by 5R01NS102272 (to J.D.D.) and F32NS105363 (to M.V.), and a microgrant from the Washington University Center for Cellular Imaging. GTAC is partially supported by P30 CA91842 and UL1TR002345 from the National Center for Advancing Translational Sciences (NCATS) of the National Institutes of Health (NIH). The content is solely the responsibility of the authors and does not necessarily represent the official view of the NIH. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
Author information
Authors and Affiliations
Contributions
Project conceptualization: M.J.V. and J.D.D. Method development: M.J.V. and Q.L. Code development: M.J.V., S.B.F. and Y.L. Validation of reagents and experiments: M.J.V., J.D.D.-J., H.W.C., S.K.K., J.Y. and Q.L. Formal analysis: M.J.V., S.M.M., S.B.F., Y.L. and J.D.D. Experiments and data collection: M.J.V., S.M.M., J.D.D.-J., H.W.C., S.K.K. and J.Y. Data curation: S.B.F. and Y.L. Writing—first draft: M.J.V., S.M.M. and S.B.F. Review and editing: M.J.V., S.K.K. and J.D.D. Figures and data visualization: M.J.V., S.M.M., S.B.F., Y.L., J.Y. and J.D.D. Oversight: Q.L. and J.D.D. Project coordination: M.J.V. and J.D.D. Funding acquisition: M.J.V. and J.D.D.
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J.D.D. has previously received royalties related to TRAP. The other authors declare no competing interests.
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Nature Neuroscience thanks Marie-Ève Tremblay and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Extended data
Extended Data Fig. 1 Synaptosomal samples show RPL10a-eGFP, enrichment of synaptophysin (SYP), and depletion of nuclear proteins.
a, Western Blot using anti-GFP antibody detects the presence of the RPL10a-eGFP fusion protein (52 kDa) within 3 independent replicates of both Input and SN-Input fractions as described in Fig. 2 and methods. b, Western Blot using anti-SYP antibody detects the neuronal presynaptic protein, SYP (34 kDa), within three independent replicates’ SN-Input fractions. c-d, Western Blots show the detection of nuclear proteins, Mecp2 (c, 75 kDa with post-translational modifications) and Lamin B1 (d, 66 kDa) within the raw cortical homogenate (Isolated before the 1000 g spin in the TRAP protocol), but shows their depletion within Input and SN-input fractions relative to the raw homogenate (two independent sets of replicates).
Extended Data Fig. 2 MG-TRAP yields a tamoxifen-dependent enrichment of microglial transcripts.
Median fold-change (FC) expression (MG-TRAP compared to Input) of the top 20–29 marker genes per cell type (as reported by Zhang et al., see Extended Data Table 4) from batch one replicate RNAseq experiments with (green dots) and without (black dots) tamoxifen injections reveals specific enrichment of microglial marker gene expression.
Extended Data Fig. 3 Multiplex in situ hybridization (ISH) shows transcript localization for PeMP and non-PeMP transcripts.
Maximum intensity projections of a 2 µm Z-stack image from ISH on p28 C57Bl/6 cortex, hippocampus, and corpus callosum tissue, for simultaneous PeMP-enriched vs. non-PeMP-enriched transcript detection in tandem with IBA1 immunofluorescence. Probes for PeMP-enriched transcripts shown in magenta and probes from non-PeMP-enriched transcripts shown in cyan. White arrows depict non-microglial signal emanating from somal-enriched probes, Kdm6b (a) and Ubash3b (b), while white arrowheads depict non-microglial signal emanating from PeMP-enriched probe, Plxnb1 (b). Images were also taken from negative control probes (d) to assess background signal levels. Quantifications are shown in Fig. 2k-l. Representative images shown from n = 5 mice and at least 4 z-stacks per brain region per mouse.
Extended Data Fig. 4 PeMP-detectable transcripts’ proteins have a higher probability of secretion using Signal-P algorithm.
Predicted secretory signal peptide probablity is higher in PeMP than in Somal microglial transcripts. N = 200 somal and 279 PeMP transcripts. p = 3.2 × e-9 by two-tailed wilcoxon ranked sum test. Box plot elements: center line, median; box limits, upper and lower quartiles; whiskers, 1.5× interquartile range; points, data points beyond the 1.5× interquartile range.
Extended Data Fig. 5 Translation blockade does not affect microglial somal size, or somal CD68 and RPL10a expression.
a-f) Whole mount immunostains were prepared from acute slices as in Fig. 4a-i. a-e, No significant differences were detected between anisomycin and vehicle-treated slices in measurements of somal area (a, p = 0.89 by unpaired two-tailed t-test), somal CD68 mean fluorescence intensity (MFI) levels normalized to whole image CD68 MFI (b, p = 0.43 by unpaired two-tailed t-test with Welch’s correction), somal CD68 pixel intensity summation (c, p = 0.72 by unpaired two-tailed t-test), somal RPL10a-GFP MFI (d, p = 0.88 by unpaired two-tailed t-test), and somal CD68 MFI at RPL10a-GFP colocalized loci (e, p = 0.99 by unpaired two-tailed t-test with Welch’s correction). f, There was no statistical difference between vehicle-treated microglial somal CD68 MFI among those supporting either 0, 1, or 2 or more PeMP-NNCs > 10 um2 in area. p = 0.69 by one-way ANOVA. a-e, N = 8 vehicle and 10 anisomycin slices with at least 4 z-stack images per slice, derived from n = 3 mice. f, N = 34 microglial somata imaged from 4 independent vehicle-treated slices per group with at least 4 z-stack images per slice. Data are shown as mean ± s.e.m.
Extended Data Fig. 6 Translation blockade does not affect cleaved caspase 3 staining in acute slice setting.
a) Whole mount immunostains were prepared from acute slices as in Fig. 4a-i except immunostained with TMEM119, cleaved Caspase 3, and DAPI. Two slices were treated with 3% ethanol (30 minute treatment) as a positive control. A TMEM119+ microglial soma (white arrow) that has a PeMP encircling and forming a phagocytic cup around a cleaved caspase 3 positive apoptotic non-microglial cell (red arrow) within the ethanol-treated group. Images representative of 2 independent experiments. b-c, No significant differences were detected between anisomycin and vehicle-treated slices in measurements of cleaved caspase-3 postive area (b, p = 0.82 by unpaired two-tailed t-test), or cleaved caspase-3 colocalized with microglial marker, TMEM119 (c, p = 0.26 by unpaired two-tailed t-test). N = 9 vehicle, n = 7 anisomycin, and n = 2 ethanol treated slices derived from n = 2 mice processed and stained on separate days. Data are shown as mean ± s.e.m.
Supplementary information
Supplementary Video 1
3D movie with a 360° view of RPS16 expression masked within the processes and soma of an IBA1+ cell. 3D reconstruction using Imaris software of z-stack images from an immunostaining for IBA1 (cyan), RPS16 (magenta; masked on IBA1 channel),and DAPI (blue) derived from 4-week-old mouse cortex. The first half of the movie shows a standard fluorescence view, while the second half shows a space-filled render on thresholded IBA1, RPS16 and DAPI channels.
Supplementary Video 2
3D movie with a 360° view showing ribosomal subunits and protein synthesis within a PeMP that is phagocytosing a neighboring cell. 3D reconstruction displayed with a space-filled rendering algorithm using Imaris software of z-stack images from a whole-mount immunostaining for IBA1 (magenta), puromycin (cyan; masked on IBA1 channel), RPL10a-eGFP (yellow) and DAPI (blue) derived from 4-week-old mouse cortex. The microglia’s soma is shown at the center, whereas the DAPI+ nucleus in the corner is nearly 100% engulfed by a microglial process. The PeMP contacting and phagocytosing a neighboring nucleus (PeMP-NNC) shows high levels of puromycin and RPL10a-eGFP staining compared to a PeMP with no contacts (opposite corner).
Supplementary Video 3
3D movie with a 360° view showing ribosomal subunits and protein synthesis within a PeMP-NNC. 3D reconstruction displayed with a space-filled rendering algorithm using Imaris software of z-stack images from a whole-mount immunostaining for IBA1 (magenta), puromycin (cyan; masked on IBA1 channel), RPL10a-eGFP (yellow) and DAPI (blue) derived from 4-week-old mouse cortex. The microglia can be seen with a long PeMP making contact with an IBA1-negative cell. The PeMP contacting this neighboring nucleus (PeMP-NNC) shows high levels of puromycin and RPL10a-eGFP staining compared to a PeMP with no contacts like the PeMP above the microglial soma.
Supplementary Video 4
Primary in vitro microglia phagocytose pathogen-like particles following vehicle treatment. Time-lapse movie taken every 10 min for 4 h with phase and green fluorescence overlay showing primary rat microglia at 7 d in vitro. Vehicle (0.9% DMSO) was added at 5 min and pHRODO-tagged E. coli BioParticles (green) were added at 35 min. Data are quantified in Fig. 5e.
Supplementary Video 5
Translation blockade slows and abrogates microglial phagocytosis in vitro by time lapse. Time-lapse movie taken every 10 min for 4 h with phase and green fluorescence overlay showing primary rat microglia at 7 d in vitro. Anisomycin (dissolved in 0.9% DMSO) was added at 5 min and pHRODO-tagged E. coli BioParticles (green) were added at 35 min. Data are quantified in Fig. 5e.
Supplementary Video 6
PeMPs severed from their somata during acute live slicing surround opsonized beads and upregulate marker of de novo protein synthesis. A descending series of 40 z-stack images (shown at teo images per second, 0.667 µm between steps) taken from 4 µm above the surface down to 22.7 µm below the surface of an acute-live slice that has been treated with opsonized beads and puromycin and then whole-mount immunostained for TMEM119 (yellow), puromycin (cyan), rabbit IgG opsonized beads (magenta) and DAPI (dark blue). There are several TMEM119+ PeMPs surrounding opsonized beads at the slice surface that cannot be traced to somata deeper within the section indicating that these PeMPs were severed from their somata in the slicing process.
Supplementary Video 7
De novo protein synthesis within PeMPs in vehicle-treated acute slices. A 3D rendering of z-stack images taken from surface and underlying 20 µm within the cortex of an acute-live slice that has been treated with opsonized beads and puromycin and then whole-mount immunostained for TMEM119 (yellow), puromycin (cyan), rabbit IgG opsonized beads (magenta) and DAPI (dark blue).
Supplementary Video 8
De novo protein synthesis within PeMPs is blocked in anisomycin-treated acute slices. A 3D rendering of z-stack images taken from surface and underlying 20 µm within the cortex of an acute-live slice that was treated with opsonized beads and puromycin and then whole-mount immunostained for TMEM119 (yellow), puromycin (cyan), rabbit IgG opsonized beads (magenta) and DAPI (dark blue).
Supplementary Table 1
RNA-seq differential expression tables including the transcripts significantly enriched by MG-TRAP and highlighting the PeMP-detectable and somal subsets. Sheet names correspond to the two sample groups subject to the differential expression analysis performed. Table contains common gene symbol (external gene name), official Ensembl gene ID, and edgeR output comparing the two groups listed in the sheet title. logFC, log2fold change for enrichment when comparing the two groups in the sheet title. P values were calculated using likelihood ratio tests and FDR (Benjamini–Hochberg) correction. For the ‘Microglial genes with location’ sheet, only samples with log2 CPM > 1, FC > 0 and corrected P value < 0.05 were included. Columns: Location: somal, PeMP or neither (NA) as defined in Fig. 2 and Methods. Unfiltered data are available at the Gene Expression Omnibus under accession no. GSE161460.
Supplementary Table 2
Supplemental Table of clueGO full output for GO term biological process PeMP versus MG-TRAP and somal versus MG-TRAP genes. GO term biological processes associated with PeMP and somal-enriched (separate tabs) microglial genes were calculated using the ClueGO plug-in51 for Cytoscape (see Methods for settings) using the full microglial gene list (Supplementary Table 1) as a custom background and tested by FDR-corrected (Benjamini–Hochberg) two-sided hypergeometric test. Column headers are defined by ClueGO. Only GO terms with corrected P < 0.05 are listed. Coloration/term groupings match those in Fig. 3a,b. Within the PeMP-enriched list, GO term grouping was only carried out on terms with a corrected P value < 0.02 to match those in Fig. 3a.
Supplementary Table 3
Nucleotide motifs enriched in somal and PeMP gene lists. Column headers are as defined by the output generated by Transite. Transite was run comparing the PeMP list to all TRAP-enriched genes (columns d–f and j), and the somal list to all TRAP-enriched genes (columns g, h and k). A Fisher’s exact test (column k) was used to identify motifs that were found more in PeMP or somal lists than expected by chance and corrected for multiple testing by Benjamin–Hochberg FDR (column p). Only FDR < 0.05 were retained. Ratio of motif enrichments was also calculated (column m). Results of hierarchical clustering (based on motif sequences position weight matrices) are also included (columns r and s).
Source data
Source Data Fig. 1
Source data from imaging quantifications.
Source Data Fig. 2
Source data from imaging quantifications.
Source Data Fig. 4
Source data from imaging quantifications.
Source Data Fig. 5
Source data from imaging quantifications.
Source Data Extended Data Fig. 1
Unmodified western blots.
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Vasek, M.J., Mueller, S.M., Fass, S.B. et al. Local translation in microglial processes is required for efficient phagocytosis. Nat Neurosci 26, 1185–1195 (2023). https://doi.org/10.1038/s41593-023-01353-0
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DOI: https://doi.org/10.1038/s41593-023-01353-0
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