Cells of the adult human heart methods
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COVID-19 and GWAS disease relevance
We define cells enriched for genes from 12 cardiovascular genome-wide association studies (GWAS) and involved in SARS-CoV-2 infection using MAGMA (Extended Data Fig. ). Atrial fibrillation GWAS signals are associated with transcriptional profiles in vCM3, owing to higher mean expression of CAV1, CAV2 and PRRX1. PR interval GWAS signals are associated with vCM3 and aCM5, with high expression of SCN5A, CAV1, ARHGAP24, MEIS1, TBX5 and TTN. GWAS signals for QRS duration are associated with specific gene expression in NC2 ( PRKCA, CEP85L, SLC35F1, SIPA1L1, KLF12 and FADS2 ). Coronary artery disease and hypertension GWAS signals are associated with transcripts from many cell lineages, particularly SMCs, FBs, and ECs, reflecting the relevance of vascular cells in both disorders.
Research ethics for donor tissues
Heart tissues (donors D1-D7 and D11) were processed at Wellcome Sanger Institute (Hinxton, UK) and obtained from deceased transplant organ donors after Research Ethics Committee approval (ref 15/EE/0152, East of England Cambridge South Research Ethics Committee) and informed consent from the donor families. Heart tissues (donors H2-H7) were processed at Harvard Medical School (Boston, Massachusetts, USA) and obtained from deceased organ donors after Human Research Ethics Board approval Pro00011739 (University of Alberta, Edmonton, Canada). Informed consent from donor families was acquired via the institutional Human Organ Procurement and Exchange Program (HOPE). Cardiovascular history was unremarkable for all donors (Supplementary Table ).
Single nuclei isolation
Single nuclei were obtained from flash-frozen tissues using mechanical homogenization as previously described. Tissues were homogenized using a 7 ml glass Dounce tissue grinder set (Merck) with 8-10 strokes of a loose pestle (A) and 8-10 strokes of a tight pestle (B) in homogenization buffer (250 mM sucrose, 25 mM KCl, 5 mM MgCl 2, 10 mM Tris-HCl, 1 mM dithiothreitol (DTT), 1 × protease inhibitor, 0.4 U µl -1 RNaseIn, 0.2 U µl -1 SUPERaseIn, 0.1% Triton X-100 in nuclease-free water). Homogenate was filtered through a 40-µm cell strainer (Corning). After centrifugation (500 g, 5 min, 4 °C) the supernatant was removed and the pellet was resuspended in storage buffer (1 × PBS, 4% bovine serum albumin (BSA), 0.2 U µl -1 Protector RNaseIn). Nuclei were stained with NucBlue Live ReadyProbes Reagents (ThermoFis...
Single-cell preparation
Heart tissues (0.2-0.9 g) were transferred from cardioplegic solution into gentleMACS C-tubes (Miltenyi Biotec) containing enzymatic digestion base solution (100 µg ml -1 liberase TH Research grade and 50 µg ml -1 DNase I, HBSS 10 mM HEPES and 30 mM taurine). Tissues were minced using scissors (FST) and automatically digested using gentleMACS Octo Dissociator (Miltenyi Biotec) with heaters. Cardiomyocyte-depleted single-cell suspension were washed with base solution containing 20% fetal bovine serum (FBS) (Gibco), filtered through 70-µm nylon strainer (BD Falcon), collected by centrifugation (330 g, 10 min, 4 °C) and resuspended in base solution containing 0.2% FBS (Gibco). Cells were manually counted three times by Trypan blue exclusion after each centrifugation and resuspended at a concentration of at least 2 × 1...
CD45 + cell enrichment
Cell suspension was prepared as described above and subsequently labelled using anti-human CD45 monoclonal antibody-conjugated microbeads according to the manufacturer's protocol (Miltenyi Biotec). In brief, up to 10 7 cells were incubated for 15 min at 4 °C in 80 µl of PBS, BSA, EDTA buffer (1 × PBS pH 7.2, 0.5% BSA, 2 mM EDTA) containing 20 µl CD45 microbeads. Cell suspension was washed in PBS, BSA, EDTA buffer once and collected by centrifugation (330 g, 10 min, 4 °C). Resuspended cells were applied to MACS LS columns (Miltenyi Biotec). CD45-depleted cell fraction was discarded after three washes with PBS, BSA and EDTA buffer and the CD45 + cell fraction was collected in PBS, BSA and EDTA buffer by removal of the columns from the magnetic field. CD45 + cells were counted and resuspended in PBS, BSA and EDTA buffer to a concentration of...
Nuclei isolation for skeletal muscle
Muscle tissue was washed in 1 × PBS, cleaned of any visible fat depositions and minced to obtain fragments of approximately 1 mm 3. Per sample, approximately 0.3 g of minced tissues was homogenized in 3 ml of buffer A (250 mM sucrose, 10 mg ml -1 BSA, 5 mM MgCl 2, 0.12 U µl -1 RNaseIn, 0.06 U µl -1 SUPERasIn, 1 × protease inhibitor) using Dounce tissue grinder set (Merck) with 50 strokes of the loose pestle (A). The homogenate was filtered through a 100-µm cell strainer (Corning) and the strainer was washed with 1 ml and then 750 µl of buffer A. After the addition of Triton X-100 (final concentration 0.5%), the mixture was further homogenized with 50 strokes of the tight pestle (B). After filtering through a 40-µm strainer, nuclei were centrifuged (3,000 g, 5 min, 4 °C), resuspended in 1 ml of buffer B (320 mM sucro...
Single-cell isolation for skeletal muscle
Muscle tissue was washed in 1 × PBS, cleaned of any visible fat depositions and finely minced. Then, 2 g of the minced tissue was transferred to digestion buffer 1 (750 U ml -1 collagenase type 2 in 1 × PBS) and incubated at 37 °C in a water bath for 90 min. The partially digested tissue was collected by centrifugation (650 g, 5 min, 4 °C) and the pellet was resuspended in digestion buffer 2 (100 U ml -1 collagenase type 2, 2 U ml -1 dispase in PBS). After 30 min incubation at 37 °C in a water bath, the digestion was stopped by the addition of 2% FBS. Cells were filtered through a 100-µm and a 40-µm nylon strainer (BD Falcon), collected by centrifugation (650 g, 4 °C, 3 min) and washed with 1 × PBS, 2% FBS. Subsequently, a 20% Percoll gradient (15,000 g, 4 °C, 20 min) was used for ce...
Extended data figures and tables
Extended Data Fig. 10 Relevance for COVID-19 and GWAS studies. a, Global expression (log 2 FC) of ACE2 in all cardiac cells. b - d, Gene expression of ACE2, TMPRSS2, CTSB and CTSL in cardiomyocytes ( b ), FBs ( c ) and vascular cells ( d ). e, Multiplexed smFISH expression of DCN (cyan), KCNJ8 (green) and ACE2 (red), nuclei are DAPI-stained (dark blue) marking fibroblasts (#; expression of DCN ) and pericytes (*; co-expression of DCN and KCNJ8 ) in right ventricular tissue section. Scale bars, 5 µm. For statistics and reproducibility, see. f, The colour coding of the heat map shows the -log 10 ( P value) of the MAGMA GWAS enrichment analysis for the association between cell type-specific expression ( y axis) and GWAS signals ( x axis). The cell types refer to the subcluster annotations and GWAS studies refer to Supplementary Table. AF, atrial fibri...
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Protein expression by western blot
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Quantify the primary readouts for this experiment: Protein expression by western blot.
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Report representative outputs alongside summary comparisons for Protein expression by western blot.
inferred from protocolSource and audit
What supports the facts on this page?
Evidence quotes (8)
We define cells enriched for genes from 12 cardiovascular genome-wide association studies (GWAS) and involved in SARS-CoV-2 infection using MAGMA (Extended Data Fig. ). Atrial fibrillation GWAS signals are associated with transcriptional profiles in vCM3, owing to higher mean expression of CAV1, CAV2 and PRRX1. PR interval GWAS signals are associated with vCM3 and aCM5, with high expression of SCN5A, CAV1, ARHGAP24, MEIS1, TBX5 and TTN. GWAS signals for QRS duration are associated with specific gene expression in NC2 ( PRKCA, CEP85L, SLC35F1, SIPA1L1, KLF12 and FADS2 ). Coronary artery disease and hypertension GWAS signals are associated with transcripts from many cell lineages, particularly SMCs, FBs, and ECs, reflecting the relevance of vascular cells in both disorders.
Heart tissues (donors D1-D7 and D11) were processed at Wellcome Sanger Institute (Hinxton, UK) and obtained from deceased transplant organ donors after Research Ethics Committee approval (ref 15/EE/0152, East of England Cambridge South Research Ethics Committee) and informed consent from the donor families. Heart tissues (donors H2-H7) were processed at Harvard Medical School (Boston, Massachusetts, USA) and obtained from deceased organ donors after Human Research Ethics Board approval Pro00011739 (University of Alberta, Edmonton, Canada). Informed consent from donor families was acquired via the institutional Human Organ Procurement and Exchange Program (HOPE). Cardiovascular history was unremarkable for all donors (Supplementary Table ).
Single nuclei were obtained from flash-frozen tissues using mechanical homogenization as previously described. Tissues were homogenized using a 7 ml glass Dounce tissue grinder set (Merck) with 8-10 strokes of a loose pestle (A) and 8-10 strokes of a tight pestle (B) in homogenization buffer (250 mM sucrose, 25 mM KCl, 5 mM MgCl 2, 10 mM Tris-HCl, 1 mM dithiothreitol (DTT), 1 × protease inhibitor, 0.4 U µl -1 RNaseIn, 0.2 U µl -1 SUPERaseIn, 0.1% Triton X-100 in nuclease-free water). Homogenate was filtered through a 40-µm cell strainer (Corning). After centrifugation (500 g, 5 min, 4 °C) the supernatant was removed and the pellet was resuspended in storage buffer (1 × PBS, 4% bovine serum albumin (BSA), 0.2 U µl -1 Protector RNaseIn). Nuclei were stained with NucBlue Live ReadyProbes Reagents (ThermoFisher) and Hoechst-positive single nuclei were purified by fluorescent activated cell sorting (FACS) using influx, XDP or FACSAria (BD Biosciences) (Supplementary Fig. ). Nuclei purification and integrity was verified under a microscope, and nuclei were further processed using the Chromium Controller...
Heart tissues (0.2-0.9 g) were transferred from cardioplegic solution into gentleMACS C-tubes (Miltenyi Biotec) containing enzymatic digestion base solution (100 µg ml -1 liberase TH Research grade and 50 µg ml -1 DNase I, HBSS 10 mM HEPES and 30 mM taurine). Tissues were minced using scissors (FST) and automatically digested using gentleMACS Octo Dissociator (Miltenyi Biotec) with heaters. Cardiomyocyte-depleted single-cell suspension were washed with base solution containing 20% fetal bovine serum (FBS) (Gibco), filtered through 70-µm nylon strainer (BD Falcon), collected by centrifugation (330 g, 10 min, 4 °C) and resuspended in base solution containing 0.2% FBS (Gibco). Cells were manually counted three times by Trypan blue exclusion after each centrifugation and resuspended at a concentration of at least 2 × 10 6 ml -1. Single cells were processed using Chromium Controller (10X Genomics) according to the manufacturer's protocol.
Cell suspension was prepared as described above and subsequently labelled using anti-human CD45 monoclonal antibody-conjugated microbeads according to the manufacturer's protocol (Miltenyi Biotec). In brief, up to 10 7 cells were incubated for 15 min at 4 °C in 80 µl of PBS, BSA, EDTA buffer (1 × PBS pH 7.2, 0.5% BSA, 2 mM EDTA) containing 20 µl CD45 microbeads. Cell suspension was washed in PBS, BSA, EDTA buffer once and collected by centrifugation (330 g, 10 min, 4 °C). Resuspended cells were applied to MACS LS columns (Miltenyi Biotec). CD45-depleted cell fraction was discarded after three washes with PBS, BSA and EDTA buffer and the CD45 + cell fraction was collected in PBS, BSA and EDTA buffer by removal of the columns from the magnetic field. CD45 + cells were counted and resuspended in PBS, BSA and EDTA buffer to a concentration of at least 2 × 10 6 per ml before further processing using a Chromium Controller (10X Genomics) according to the manufacturer's protocol.
Muscle tissue was washed in 1 × PBS, cleaned of any visible fat depositions and minced to obtain fragments of approximately 1 mm 3. Per sample, approximately 0.3 g of minced tissues was homogenized in 3 ml of buffer A (250 mM sucrose, 10 mg ml -1 BSA, 5 mM MgCl 2, 0.12 U µl -1 RNaseIn, 0.06 U µl -1 SUPERasIn, 1 × protease inhibitor) using Dounce tissue grinder set (Merck) with 50 strokes of the loose pestle (A). The homogenate was filtered through a 100-µm cell strainer (Corning) and the strainer was washed with 1 ml and then 750 µl of buffer A. After the addition of Triton X-100 (final concentration 0.5%), the mixture was further homogenized with 50 strokes of the tight pestle (B). After filtering through a 40-µm strainer, nuclei were centrifuged (3,000 g, 5 min, 4 °C), resuspended in 1 ml of buffer B (320 mM sucrose, 10 mg ml -1 BSA, 3 mM CaCl 2, 2 mM magnesium acetate, 0.1 mM EDTA, 10 mM Tris-HCl, 1 mM DTT, 1 × protease inhibitor, 0.12 U µl -1 RNaseIn, 0.06 U µl -1 SUPERasin) and purified using a 27% Percoll gradient solution. The Percoll mixture was centrifuged at...
Muscle tissue was washed in 1 × PBS, cleaned of any visible fat depositions and finely minced. Then, 2 g of the minced tissue was transferred to digestion buffer 1 (750 U ml -1 collagenase type 2 in 1 × PBS) and incubated at 37 °C in a water bath for 90 min. The partially digested tissue was collected by centrifugation (650 g, 5 min, 4 °C) and the pellet was resuspended in digestion buffer 2 (100 U ml -1 collagenase type 2, 2 U ml -1 dispase in PBS). After 30 min incubation at 37 °C in a water bath, the digestion was stopped by the addition of 2% FBS. Cells were filtered through a 100-µm and a 40-µm nylon strainer (BD Falcon), collected by centrifugation (650 g, 4 °C, 3 min) and washed with 1 × PBS, 2% FBS. Subsequently, a 20% Percoll gradient (15,000 g, 4 °C, 20 min) was used for cell purification. The layer containing cells was collected, washed in PBS containing 2% FBS, and viable cells were counted by Trypan Blue exclusion using a haemocytometer. Nuclei were profiled using a Chromium Controller (10X Genomics) according to the manufacturer's protocol.
Extended Data Fig. 10 Relevance for COVID-19 and GWAS studies. a, Global expression (log 2 FC) of ACE2 in all cardiac cells. b - d, Gene expression of ACE2, TMPRSS2, CTSB and CTSL in cardiomyocytes ( b ), FBs ( c ) and vascular cells ( d ). e, Multiplexed smFISH expression of DCN (cyan), KCNJ8 (green) and ACE2 (red), nuclei are DAPI-stained (dark blue) marking fibroblasts (#; expression of DCN ) and pericytes (*; co-expression of DCN and KCNJ8 ) in right ventricular tissue section. Scale bars, 5 µm. For statistics and reproducibility, see. f, The colour coding of the heat map shows the -log 10 ( P value) of the MAGMA GWAS enrichment analysis for the association between cell type-specific expression ( y axis) and GWAS signals ( x axis). The cell types refer to the subcluster annotations and GWAS studies refer to Supplementary Table. AF, atrial fibrillation; CAD, coronary artery disease; HF, heart failure; HR, heart rate; HT, hypertension; LVD, left ventricular diameter; NICM, non-ischaemic cardiomyopathy; PR, PR interval; PWAVE, P-wave duration; T2D, type 2 diabetes; QRS, QRS complex duration; QT, QT interval. Dots mark significant association...
Machine-readable layer
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"text": "Extended Data Fig. 10 Relevance for COVID-19 and GWAS studies. a, Global expression (log 2 FC) of ACE2 in all cardiac cells. b - d, Gene expression of ACE2, TMPRSS2, CTSB and CTSL in cardiomyocytes ( b ), FBs ( c ) and vascular cells ( d ). e, Multiplexed smFISH expression of DCN (cyan), KCNJ8 (green) and ACE2 (red), nuclei are DAPI-stained (dark blue) marking fibroblasts (#; expression of DCN ) and pericytes (*; co-expression of DCN and KCNJ8 ) in right ventricular tissue section. Scale bars, 5 µm. For statistics and reproducibility, see. f, The colour coding of the heat map shows the -log 10 ( P value) of the MAGMA GWAS enrichment analysis for the association between cell type-specific expression ( y axis) and GWAS signals ( x axis). The cell types refer to the subcluster annotations and GWAS studies refer to Supplementary Table. AF, atrial fibri..."
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