Microglia regulate central nervous system myelin growth and integrity methods
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SRI-011381 hydrochloride administration
The TGFβ signalling agonist SRI-011381 hydrochloride (HY-100347A, Cambridge Bioscience/MedChem Express), dissolved in PBS containing DMSO (10%) and PEG300 (40%), was injected intraperitoneally into Fire Δ/Δ mice at a dose of 30 mg kg -1 3 times per week for 3 weeks (9 injections in total) and killed as described above.
Behavioural testing
Experimenters were blinded to genotype during behavioural testing and data analyses. All experiments were performed in a behaviour testing room maintained at a constant temperature of 20 °C. The open-field test was performed on male mice at 4-8 weeks and 11-13 months of age to assess locomotor activity and anxiety-associated behaviours. Handling was carried out 3-4 days before testing. Mice were placed in the open field (47 × 47 cm) to freely explore the arena for 10 min. Equipment was cleaned with 70% ethanol between each test to remove odours. The total ambulatory distance travelled (in metres) and the time spent in the edges (9 cm from the wall) and centre (29 × 29 cm) were automatically quantified using the video tracking software Any-Maze (Stoelting Europe, v.6.3). The Barnes...
Immunofluorescence staining of mouse tissue
Mice were intracardially perfused with 4% paraformaldehyde (PFA; w/v; Sigma), and brains were post-fixed overnight and cryoprotected in sucrose before embedding in OCT (Tissue-Tech) and storage at -80 °C. Cryosections (10 µm) were air-dried, permeabilized and blocked for 1 h with 5% normal horse serum (Gibco) and 0.3% Triton-X-100 (Fisher Scientific) in PBS. For myelin protein staining, sections were permeabilized in methanol at -20 °C for 10 min. For EdU visualization, an AlexaFluor-555 Click-iT EdU Cell Proliferation Assay kit (Invitrogen) was applied before immunostaining. Sections were permeabilized with 0.5% Triton X-100 in PBS for 20 min at room temperature (20-25 °C) then incubated in Click-iT reaction cocktail in the dark at room temperature for 30 min and then washed in PBS. Heat-induc...
Measuring TGFβ1 levels by ELISA
Following perfusion with PBS, the corpus callosum was dissected from 2 mm coronal sections of Fire Δ/Δ and wild-type brains and snap-frozen in liquid nitrogen. Samples were homogenized in RIPA buffer (Millipore, 20-188) containing phosphatase and protease inhibitors (Sigma-Aldrich, 4906845001 and 11836170001). Corpus callosum lysate samples were activated and TGFβ1 protein levels were measured by ELISA (BioLegend, 436707) according to the manufacturer's instructions for serum and plasma samples at a final dilution of 1:10. BCA assays were performed to measure total protein according to the manufacturer's instructions (Thermo Fisher Scientific, 23225), and values were normalized to this for each sample.
Lipidomics
Corpus callosum samples from Fire +/+ and Fire Δ/Δ mice were diluted in 700 µl of PBS with 800 µl 1 N HCl:CH 3 OH 1:8 (v/v), 900 µl ChCl 3 and 200 µg ml -1 of the antioxidant 2,6- di -tert-butyl-4-methylphenol (BHT; Sigma-Aldrich). Splash Lipidomix Mass Spec standard (3 µl; Avanti Polar Lipids) was added into the extract mix. The organic fraction was evaporated at room temperature using a Savant Speedvac spd111v (Thermo Fisher), and the remaining lipid pellet was reconstituted in 100% ethanol. Lipid species were analysed by liquid chromatography electrospray ionization tandem mass spectrometry (LC-ESI-MS/MS) on a Nexera X2 UHPLC system (Shimadzu) coupled with hybrid triple quadrupole/linear ion trap mass spectrometer (6500+ QTRAP system; AB SCIEX). Chromatographic separation was performed on...
Immunofluorescence staining of human tissue
Post-mortem tissue from individuals with ALSP and from unaffected individuals who had died of non-neurological causes (Extended Data Table ) were obtained with full ethical approval from the Queen Square Brain Bank for Neurological Disorders, UCL Queen Square Institute of Neurology, and their use was in accord with the terms of the informed consents for use of donor tissue and information. Ethical approval was granted to the Queen Square Brain Bank for the use of tissue by the National Health Service Health Research Authority through the London Central Research Ethics Committee. Diagnosis of ALSP was confirmed on the basis of mutations in CSF1R and by neuropathological means, and clinical history was provided by Z. Jaunmuktane (University College London). Formalin-fixed paraffin embedded tissue blocks were cut to 10 µm thickness. Sections were placed in the oven at 60...
Extended data figures and tables
Extended Data Fig. 4 Learning and memory encoding unimpaired, but cognitive flexibility is compromised, in the FIRE Δ/Δ mouse. a ) Training phase of Barnes maze: mice learn to locate Target hole 1 (orange) with underlying escape chamber in spatial learning and memory retrieval trials. Mice tested were 2-4 months of age, with a median age of 119 days old (FIRE +/+ ) and 120 days old (FIRE Δ/Δ ). b ) Mean primary latency (sec) ± s.e.m. over 6 training days. n = 13 FIRE +/+ mice and 10 FIRE Δ/Δ. Non-significant between genotypes across all training days, Day 1: ** P = 0.0011; Day 2: P = 0.9787; Day 3: P = 0.9627; Day 4: P = 0.9574; Day 5: P = 0.9990; Day 6: P > 0.9999, Repeated measures 2-way ANOVA with Sidak's multiple comparisons test. c ) Mean prima...
Extended data figures and tables
Extended Data Fig. 5 Post-learning oligodendrogenesis and myelination. a ) Representative images of EdU (magenta) and OLIG2 (white) double positive cells (arrows), with magnified view of dotted outline. Scale bars, 25 µm. b ) Mean OLIG2+ EdU+ cells/mm 2 ± s.e.m. n = 9 FIRE +/+ mice and 4 FIRE Δ/Δ mice. Non-significant, P = 0.9696, 2-tailed unpaired Student's t-test. c ) Mean proportion of OLIG2+ EdU+ cells which are mature oligodendrocytes (CC1+; black) or immature lineage cells (CC1-; grey) ± s.e.m. n = 9 FIRE +/+ mice and 4 FIRE Δ/Δ mice. Non-significant, CC1+: P > 0.9999; CC1-: P > 0.9999, 1-way ANOVA with Tukey's multiple comparisons test. d ) Representative images of EdU+ (magenta) CC1+ (green) OLIG2+ (white) triple positive cells (arrows). Scale bar, 25 µm....
Measurement outputs
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Microscopy-based tissue or cell-state imaging
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Quantify the primary readouts for this experiment: Microscopy-based tissue or cell-state imaging.
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Evidence quotes (8)
The TGFβ signalling agonist SRI-011381 hydrochloride (HY-100347A, Cambridge Bioscience/MedChem Express), dissolved in PBS containing DMSO (10%) and PEG300 (40%), was injected intraperitoneally into Fire Δ/Δ mice at a dose of 30 mg kg -1 3 times per week for 3 weeks (9 injections in total) and killed as described above.
Experimenters were blinded to genotype during behavioural testing and data analyses. All experiments were performed in a behaviour testing room maintained at a constant temperature of 20 °C. The open-field test was performed on male mice at 4-8 weeks and 11-13 months of age to assess locomotor activity and anxiety-associated behaviours. Handling was carried out 3-4 days before testing. Mice were placed in the open field (47 × 47 cm) to freely explore the arena for 10 min. Equipment was cleaned with 70% ethanol between each test to remove odours. The total ambulatory distance travelled (in metres) and the time spent in the edges (9 cm from the wall) and centre (29 × 29 cm) were automatically quantified using the video tracking software Any-Maze (Stoelting Europe, v.6.3). The Barnes maze test was performed in adult mice 2-4 months of age to assess spatial learning, memory and cognitive flexibility. The maze consisted of one white circular platform with 20 circular holes around the outside edge, 91.5 cm in diameter and 115 cm in height (San Diego Instrume...
Mice were intracardially perfused with 4% paraformaldehyde (PFA; w/v; Sigma), and brains were post-fixed overnight and cryoprotected in sucrose before embedding in OCT (Tissue-Tech) and storage at -80 °C. Cryosections (10 µm) were air-dried, permeabilized and blocked for 1 h with 5% normal horse serum (Gibco) and 0.3% Triton-X-100 (Fisher Scientific) in PBS. For myelin protein staining, sections were permeabilized in methanol at -20 °C for 10 min. For EdU visualization, an AlexaFluor-555 Click-iT EdU Cell Proliferation Assay kit (Invitrogen) was applied before immunostaining. Sections were permeabilized with 0.5% Triton X-100 in PBS for 20 min at room temperature (20-25 °C) then incubated in Click-iT reaction cocktail in the dark at room temperature for 30 min and then washed in PBS. Heat-induced antigen retrieval was performed before primary antibody application. Primary antibodies were applied overnight at 4 °C in a humid chamber and included the following: MBP (AbD Serotec, 1:250; MCA409S, clone 12); MAG (Millipore, 1:100; MAB1567, clone 513); MOG (Millipore, 1:100; MAB5680,...
Following perfusion with PBS, the corpus callosum was dissected from 2 mm coronal sections of Fire Δ/Δ and wild-type brains and snap-frozen in liquid nitrogen. Samples were homogenized in RIPA buffer (Millipore, 20-188) containing phosphatase and protease inhibitors (Sigma-Aldrich, 4906845001 and 11836170001). Corpus callosum lysate samples were activated and TGFβ1 protein levels were measured by ELISA (BioLegend, 436707) according to the manufacturer's instructions for serum and plasma samples at a final dilution of 1:10. BCA assays were performed to measure total protein according to the manufacturer's instructions (Thermo Fisher Scientific, 23225), and values were normalized to this for each sample.
Corpus callosum samples from Fire +/+ and Fire Δ/Δ mice were diluted in 700 µl of PBS with 800 µl 1 N HCl:CH 3 OH 1:8 (v/v), 900 µl ChCl 3 and 200 µg ml -1 of the antioxidant 2,6- di -tert-butyl-4-methylphenol (BHT; Sigma-Aldrich). Splash Lipidomix Mass Spec standard (3 µl; Avanti Polar Lipids) was added into the extract mix. The organic fraction was evaporated at room temperature using a Savant Speedvac spd111v (Thermo Fisher), and the remaining lipid pellet was reconstituted in 100% ethanol. Lipid species were analysed by liquid chromatography electrospray ionization tandem mass spectrometry (LC-ESI-MS/MS) on a Nexera X2 UHPLC system (Shimadzu) coupled with hybrid triple quadrupole/linear ion trap mass spectrometer (6500+ QTRAP system; AB SCIEX). Chromatographic separation was performed on a XBridge amide column (150 × 4.6 mm, 3 × 5 µm; Waters) maintained at 35 °C using mobile phase A (1 mM ammonium acetate in water and acetonitrile 5:95 (v/v)) and mobile phase B (1 mM ammonium acetate in water and...
Post-mortem tissue from individuals with ALSP and from unaffected individuals who had died of non-neurological causes (Extended Data Table ) were obtained with full ethical approval from the Queen Square Brain Bank for Neurological Disorders, UCL Queen Square Institute of Neurology, and their use was in accord with the terms of the informed consents for use of donor tissue and information. Ethical approval was granted to the Queen Square Brain Bank for the use of tissue by the National Health Service Health Research Authority through the London Central Research Ethics Committee. Diagnosis of ALSP was confirmed on the basis of mutations in CSF1R and by neuropathological means, and clinical history was provided by Z. Jaunmuktane (University College London). Formalin-fixed paraffin embedded tissue blocks were cut to 10 µm thickness. Sections were placed in the oven at 60 °C for 10 min and deparaffinized by a series of washes in HistoClear (2 × 10 min) and ethanol (100% twice, 95%, 70%, 50%; 5 min each). Following washes in PBS, slides were placed in a pressure cooker in Vector unmasking solution for 20 min, cooled, washed once...
Extended Data Fig. 4 Learning and memory encoding unimpaired, but cognitive flexibility is compromised, in the FIRE Δ/Δ mouse. a ) Training phase of Barnes maze: mice learn to locate Target hole 1 (orange) with underlying escape chamber in spatial learning and memory retrieval trials. Mice tested were 2-4 months of age, with a median age of 119 days old (FIRE +/+ ) and 120 days old (FIRE Δ/Δ ). b ) Mean primary latency (sec) ± s.e.m. over 6 training days. n = 13 FIRE +/+ mice and 10 FIRE Δ/Δ. Non-significant between genotypes across all training days, Day 1: ** P = 0.0011; Day 2: P = 0.9787; Day 3: P = 0.9627; Day 4: P = 0.9574; Day 5: P = 0.9990; Day 6: P > 0.9999, Repeated measures 2-way ANOVA with Sidak's multiple comparisons test. c ) Mean primary errors ± s.e.m. during training phase. n = 13 FIRE +/+ mice and 10 FIRE Δ/Δ mice. Non-significant, Day 1: P = 0.9649; Day 2: P = 0.5968; Day 3: P = 0.8884; Day 4: P = 0.6028; Day 5: P = 0.9215; Day 6: P &#...
Extended Data Fig. 5 Post-learning oligodendrogenesis and myelination. a ) Representative images of EdU (magenta) and OLIG2 (white) double positive cells (arrows), with magnified view of dotted outline. Scale bars, 25 µm. b ) Mean OLIG2+ EdU+ cells/mm 2 ± s.e.m. n = 9 FIRE +/+ mice and 4 FIRE Δ/Δ mice. Non-significant, P = 0.9696, 2-tailed unpaired Student's t-test. c ) Mean proportion of OLIG2+ EdU+ cells which are mature oligodendrocytes (CC1+; black) or immature lineage cells (CC1-; grey) ± s.e.m. n = 9 FIRE +/+ mice and 4 FIRE Δ/Δ mice. Non-significant, CC1+: P > 0.9999; CC1-: P > 0.9999, 1-way ANOVA with Tukey's multiple comparisons test. d ) Representative images of EdU+ (magenta) CC1+ (green) OLIG2+ (white) triple positive cells (arrows). Scale bar, 25 µm. e ) Images of corpus callosum 6 weeks post cognitive testing. Scale bar, 1 µm. f ) Mean number of myelinated axons/mm 2 ± s.e.m. in untrained versus trained mice. n = 3 mice/group in untrained category, 4 trained FIRE +/+ mice and 6 trained FIRE Δ/Δ mice. FIRE...
Machine-readable layer
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"text": "Extended Data Fig. 4 Learning and memory encoding unimpaired, but cognitive flexibility is compromised, in the FIRE Δ/Δ mouse. a ) Training phase of Barnes maze: mice learn to locate Target hole 1 (orange) with underlying escape chamber in spatial learning and memory retrieval trials. Mice tested were 2-4 months of age, with a median age of 119 days old (FIRE +/+ ) and 120 days old (FIRE Δ/Δ ). b ) Mean primary latency (sec) ± s.e.m. over 6 training days. n = 13 FIRE +/+ mice and 10 FIRE Δ/Δ. Non-significant between genotypes across all training days, Day 1: ** P = 0.0011; Day 2: P = 0.9787; Day 3: P = 0.9627; Day 4: P = 0.9574; Day 5: P = 0.9990; Day 6: P > 0.9999, Repeated measures 2-way ANOVA with Sidak's multiple comparisons test. c ) Mean prima..."
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"text": "Extended Data Fig. 5 Post-learning oligodendrogenesis and myelination. a ) Representative images of EdU (magenta) and OLIG2 (white) double positive cells (arrows), with magnified view of dotted outline. Scale bars, 25 µm. b ) Mean OLIG2+ EdU+ cells/mm 2 ± s.e.m. n = 9 FIRE +/+ mice and 4 FIRE Δ/Δ mice. Non-significant, P = 0.9696, 2-tailed unpaired Student's t-test. c ) Mean proportion of OLIG2+ EdU+ cells which are mature oligodendrocytes (CC1+; black) or immature lineage cells (CC1-; grey) ± s.e.m. n = 9 FIRE +/+ mice and 4 FIRE Δ/Δ mice. Non-significant, CC1+: P > 0.9999; CC1-: P > 0.9999, 1-way ANOVA with Tukey's multiple comparisons test. d ) Representative images of EdU+ (magenta) CC1+ (green) OLIG2+ (white) triple positive cells (arrows). Scale bar, 25 µm...."
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