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Transthoracic echocardiograms to measure ventricular size, wall thickness, and ejection fraction were performed on mice using the Vevo 2,700 VisualSonics System.

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Transthoracic echocardiograms to measure ventricular size, wall thickness, and ejection fraction were performed on mice using the Vevo 2,700 VisualSonics System. Intraperitoneal injection with 0.1 mg midazolam was applied for anxiolytic muscle relaxant effects, without any anesthetic agent that may cause cardiac suppression. Standard 2D, M-mode, Doppler, Tissue Doppler images were obtained using a 30-MHz linear array transducer, including the parasternal short and long axis. All image analysis was performed by Vevo 2,100 analysis software (v.1.5) after rapid image collection. The diastolic function was measured using tissue Doppler imaging of the mitral annulus (E`) and conventional mitral inflow (E wave).

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Metabolic chamber by Promethion (Sable Systems International) was applied to characterize the metabolism of whole-animal energy expenditure.145 The 16-cage metabolic chamber system directly measures various parameters over a 72-hour period, such as heat production, oxygen consumption (VO2), CO2 production, and XY activity movement. The respiratory exchange ratio (RER) is calculated as the ratio of carbon dioxide production (VCO2) to oxygen consumption. This parameter is useful to estimate the metabolic status. The xy axis detection of animal motion measure activity during day-time and night-time. The formula applied was Heat = (1.232∗VCO2)+(3.815∗VO2).

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For generation of SURF1 KO pigs, we followed a protocol for somatic cell nuclear transfer (SCNT) based on our previous method11 with minor modifications. Briefly, ovaries from pubertal gilts of domestic pig, large white background were collected at a local abattoir and transported to the lab at 31-33 °C. Follicles larger than 3 mm were aspirated, and cumulus-oocyte complexes (COCs) were selected and matured in vitro at 38.5 °C under 5 % CO2 for 42 h. One day before SCNT, donor cells were induced into quiescence via serum starvation (0.5 % FCS). On the day of SCNT, cells were trypsinized, washed, and resuspended in SOF-Hepes medium. Intraperitoneal injection with 0.1 mg midazolam was applied for anxiolytic muscle relaxant effects, without any anesthetic agent that may cause cardiac suppression. Standard 2D, M-mode, Doppler, Tissue Doppler images were obtained using a 30-MHz linear array transducer, including the parasternal short and long axis. All image analysis was performed by Vevo 2,100 analysis software (v.1.5) after rapid image collection. The diastolic function was measured using tissue Doppler imaging of the mitral annulus (E`) and conventional mitral inflow (E wave). Metabolic chamber by Promethion (Sable Systems International) was applied to characterize the metabolism of whole-animal energy expenditure.145 The 16-cage metabolic chamber system directly measures various parameters over a 72-hour period, such as heat production, oxygen consumption (VO2), CO2 production, and XY activity movement. The respiratory exchange ratio (RER) is calculated as the ratio of carbon dioxide production (VCO2) to oxygen consumption. This parameter is useful to estimate the metabolic status. The xy axis detection of animal motion measure activity during day-time and night-time. The formula applied was Heat = (1.232∗VCO2)+(3.815∗VO2). For generation of SURF1 KO pigs, we followed a protocol for somatic cell nuclear transfer (SCNT) based on our previous method11 with minor modifications.

Briefly, ovaries from pubertal gilts of domestic pig, large white background were collected at a local abattoir and transported to the lab at 31-33 °C. Follicles larger than 3 mm were aspirated, and cumulus-oocyte complexes (COCs) were selected and matured in vitro at 38.5 °C under 5 % CO2 for 42 h.

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For biochemical and immunoblot experiments, we isolated the basal ganglia of newborn male pigs: 3 SURF1 KO, 3 SURF1 KO treated with sildenafil (2.1 mg/kg/day), and 3 sex and age-matched WT. Spectrophotometric analyses of complex IV (CIV) and citrate synthase (CS) activities were carried out as previously described.135 CIV activity was normalized to CS activity, an index of mitochondrial mass. For histological analysis, tissues were removed immediately after death, post-fixed in 4 % PFA at 4 °C for 48 h, cryoprotected in DPBS containing 30 % sucrose for 24 h at 4 °C, embedded in optimal cutting temperature (OCT) compound, and frozen on dry ice. Cryostat sections (10 μm thick) were then mounted on gelatin-coated glass slides. The sections were stained with hematoxylin and eosin (H&E).

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Images were acquired using a Nikon Eclipse E400 light microscope at 20 x or 40 x magnification. The sildenafil plasma concentration was monitored in three treated LS patients. EDTA blood was drawn in the morning before the first dose (trough level) and one hour after oral sildenafil application (peak level). Depicted time points in Figure 6D were separated by more than 3 months for each patient. The quantification was performed by Liquid Chromatography-Tandem Mass Spectrometry (LC-MS/MS).

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The EDTA-blood sample was centrifuged at 3,000 x g for 10 min at 4 °C and the plasma was aliquoted and frozen at -80 °C until measurement. Proteins were precipitated by vortexing for 1 min and subsequent sildenafil citrate 200mg price storage for 60 min at -20 °C. Supernatants were obtained by centrifugation at 16,000 x g at 4 °C for 10 min and subjected to LC-MS/MS sildenafil quantification applying the multiple reaction monitoring (MRM) approach. Water (eluent A) and acetonitrile (eluent B), both acidified with 0.1 % formic acid, were pumped with 0.4 ml/min. Elution of sildenafil and its internal standard was achieved with a 10-min linear gradient from 5 % to 90 % eluent B. One day before SCNT, donor cells were induced into quiescence via serum starvation (0.5 % FCS). On the day of SCNT, cells were trypsinized, washed, and resuspended in SOF-Hepes medium. Matured oocytes (with extruded polar body) were selected and zona pellucida was removed using 0.5 % pronase in DPBS. All manipulations were performed in SOF-Hepes with 10 % FCS.

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Enucleated cytoplasts were exposed to phytohemagglutinin and fused with donor cells via double DC-pulse (1.2 kV/cm), then returned to maturation medium. As nuclear donor, we used a cell clone obtained by homologous direct recombination (HDR)11 that harbors a 106 bp deletion on the left homology arm of exon 3 as well as a puromycin-resistance cassette in both alleles of the SURF1 gene.

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Matured oocytes (with extruded polar body) were selected and zona pellucida was removed using 0.5 % pronase in DPBS. All manipulations were performed in SOF-Hepes with 10 % FCS. Enucleated cytoplasts were exposed to phytohemagglutinin and fused with donor cells via double DC-pulse (1.2 kV/cm), then returned to maturation medium. As nuclear donor, we used a cell clone obtained by homologous direct recombination (HDR)11 that harbors a 106 bp deletion on the left homology arm of exon 3 as well as a puromycin-resistance cassette in both alleles of the SURF1 gene. Embryos were cultured in modified mSOF medium with amino acids and 4 mg/ml BSA, using a modified Well-of-the-Well system.

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Sows were synchronized with 12 mg/day of altrenogest for 15 days. On day 13, they received 0.15 mg PgF2α, followed by 1000 IU hCG 96 h after the last altrenogest dose. On day 6 of SCNT embryo development (compacted morula to early blastocyst stage), embryos were surgically transferred via mid-ventral laparotomy, five days after standing estrus. Pregnancy was assessed via ultrasound on day 30 and confirmed on day 60 post-transfer. Farrowing was induced with PgF2α on days 114-115 sildenafil spray of gestation.

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For body temperature detection we used a Thermal Imaging Camera (Dongguan Xintai Instrument Co., Ltd, China). SURF1 KO male piglets were treated immediately after birth with sildenafil citrate (n=3 animals with 2.1 mg/kg/day, n=4 animals with 0.5 mg/kg/day). At birth, the animals were separated from the sow and transferred to an incubator kept at 35 °C. Sildenafil was always administered at the same time and dissolved in milk. The veterinarian ensured that the entire dose was consumed. Embryos were cultured in modified mSOF medium with amino acids and 4 mg/ml BSA, using a modified Well-of-the-Well system. Sows were synchronized with 12 mg/day of altrenogest for 15 days. On day 13, they received 0.15 mg PgF2α, followed by 1000 IU hCG 96 h after the last altrenogest dose. On day 6 of SCNT embryo development (compacted morula to early blastocyst stage), embryos were surgically transferred via mid-ventral laparotomy, five days after standing estrus. Pregnancy was assessed via ultrasound on day 30 and confirmed on day 60 post-transfer. Farrowing was induced with PgF2α on days 114-115 sildenafil spray of gestation. For body temperature detection we used a Thermal Imaging Camera (Dongguan Xintai Instrument Co., Ltd, China). SURF1 KO male piglets were treated immediately after birth with sildenafil citrate (n=3 animals with 2.1 mg/kg/day, n=4 animals with 0.5 mg/kg/day). At birth, the animals were separated from the sow and transferred to an incubator kept at 35 °C. Sildenafil was always administered at the same time and dissolved in milk. The veterinarian ensured that the entire dose was consumed. For biochemical and immunoblot experiments, we isolated the basal ganglia of newborn male pigs: 3 SURF1 KO, 3 SURF1 KO treated with sildenafil (2.1 mg/kg/day), and 3 sex and age-matched WT. Spectrophotometric analyses of complex IV (CIV) and citrate synthase (CS) activities were carried out as previously described.135 CIV activity was normalized to CS activity, an index of mitochondrial mass. For histological analysis, tissues were removed immediately after death, post-fixed in 4 % PFA at 4 °C for 48 h, cryoprotected in DPBS containing 30 % sucrose for 24 h at 4 °C, embedded in optimal cutting temperature (OCT) compound, and frozen on dry ice. Cryostat sections (10 μm thick) were then mounted on gelatin-coated glass slides. The sections were stained with hematoxylin and eosin (H&E). Images were acquired using a Nikon Eclipse E400 light microscope at 20 x or 40 x magnification. The sildenafil plasma concentration was monitored in three treated LS patients. EDTA blood was drawn in the morning before the first dose (trough level) and one hour after oral sildenafil application (peak level). Depicted time points in Figure 6D were separated by more than 3 months for each patient. The quantification was performed by Liquid Chromatography-Tandem Mass Spectrometry (LC-MS/MS). The EDTA-blood sample was centrifuged at 3,000 x g for 10 min at 4 °C and the plasma was aliquoted and frozen at -80 °C until measurement. Proteins were precipitated by vortexing for 1 min and subsequent sildenafil citrate 200mg price storage for 60 min at -20 °C. Supernatants were obtained by centrifugation at 16,000 x g at 4 °C for 10 min and subjected to LC-MS/MS sildenafil quantification applying the multiple reaction monitoring (MRM) approach. Water (eluent A) and acetonitrile (eluent B), both acidified with 0.1 % formic acid, were pumped with 0.4 ml/min. Elution of sildenafil and its internal standard was achieved with a 10-min linear gradient from 5 % to 90 % eluent B. Total run-time was 17 min including re-equilibration of the LC system.

MS/MS analyses were carried out using an Ultivo triple-quadrupole mass spectrometer (Agilent Technologies) operating in the positive electrospray ionization mode (ESI+). The following ion source parameters were set: sheath gas temperature, 400 °C; sheath gas flow, 12 l/min of nitrogen; nebulizer pressure, 20 psi; drying gas temperature, 100 °C; drying gas flow, 7 l/min of nitrogen; capillary voltage, 3.0 kV; nozzle voltage, 0 kV. The following mass transitions were recorded (fragmentor voltage [FV] and collision energies [CE] in parentheses): sildenafil: m/z 475.2 → 58.0 (FV: 220 V, CE: 68 eV, quantifier), m/z 475.2 → 100.0 (FV: 220 V, CE: 28 eV), m/z 475.2 → 283.1 (FV: 220 V, CE: 44 eV); d3-sildenafil: m/z 478.2 → 60.9 (FV: 220 V, CE: 68 eV, quantifier), m/z 478.2 → 103.0 (FV: 220 V, CE: 28 eV), m/z 478.2 → 283.1 (FV: 220 V, CE: 44 eV). Peak areas were determined with MassHunter Software (Agilent Technologies) and sildenafil was directly quantified via its internal standard d3-sildenafil that was concentrated to 8 nM in the samples. Heteroplasmy levels and mtDNA haplotypes in the whole exome sequencing (WES) datasets were determined using the software MToolBox v.1.146,147 Results were visualized in the IGV viewer v2.16.148 Heteroplasmy levels of the MT-ATP6 mutations in fibroblasts, iPSCs, and NPCs were determined using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analysis, as described before.27 Genomic DNA was isolated using the Nucleo-Spin Tissue kit (Macherey-Nagel). We used restriction enzyme StuI (NEB, R0187, 10,000 units/ml) for the m.9185T>C mutation (wild-type: 24+90 pb, mutation: 114 pb), HpaII (NEB, R0171, 10,000 units/ml) for m.8993T>C and m.8993T>G (wild type: 25+155 bp; mutant: 180 bp), XbaI (NEB, R0145, 10,000 units/ml) for m.9176 T>G (wild type: 24+155 bp, mutant: 179 bp). The percentage of cleaved versus uncleaved fragments was determined by capillary electrophoresis and laser detection of the FAM-labelled RFLP-fragments using the 3,500 Series Genetic Analyzer (Applied Biosystems, RRID:SCR_021901) and normalized to a standard curve of known degrees of heteroplasmy.

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Total run-time was 17 min including re-equilibration of the LC system. MS/MS analyses were carried out using an Ultivo triple-quadrupole mass spectrometer (Agilent Technologies) operating in the positive electrospray ionization mode (ESI+). The following ion source parameters were set: sheath gas temperature, 400 °C; sheath gas flow, 12 l/min of nitrogen; nebulizer pressure, 20 psi; drying gas temperature, 100 °C; drying gas flow, 7 l/min of nitrogen; capillary voltage, 3.0 kV; nozzle voltage, 0 kV. The following mass transitions were recorded (fragmentor voltage [FV] and collision energies [CE] in parentheses): sildenafil: m/z 475.2 → 58.0 (FV: 220 V, CE: 68 eV, quantifier), m/z 475.2 → 100.0 (FV: 220 V, CE: 28 eV), m/z 475.2 → 283.1 (FV: 220 V, CE: 44 eV); d3-sildenafil: m/z 478.2 → 60.9 (FV: 220 V, CE: 68 eV, quantifier), m/z 478.2 → 103.0 (FV: 220 V, CE: 28 eV), m/z 478.2 → 283.1 (FV: 220 V, CE: 44 eV). Peak areas were determined with MassHunter Software (Agilent Technologies) and sildenafil was directly quantified via its internal standard d3-sildenafil that was concentrated to 8 nM in the samples.

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Heteroplasmy levels and mtDNA haplotypes in the whole exome sequencing (WES) datasets were determined using the software MToolBox v.1.146,147 Results were visualized in the IGV viewer v2.16.148 Heteroplasmy levels of the MT-ATP6 mutations in fibroblasts, iPSCs, and NPCs were determined using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analysis, as described before.27 Genomic DNA was isolated using the Nucleo-Spin Tissue kit (Macherey-Nagel). We used restriction enzyme StuI (NEB, R0187, 10,000 units/ml) for the m.9185T>C mutation (wild-type: 24+90 pb, mutation: 114 pb), HpaII (NEB, R0171, 10,000 units/ml) for m.8993T>C and m.8993T>G (wild type: 25+155 bp; mutant: 180 bp), XbaI (NEB, R0145, 10,000 units/ml) for m.9176 T>G (wild type: 24+155 bp, mutant: 179 bp). The percentage of cleaved versus uncleaved fragments was determined by capillary electrophoresis and laser detection of the FAM-labelled RFLP-fragments using the 3,500 Series Genetic Analyzer (Applied Biosystems, RRID:SCR_021901) and normalized to a standard curve of known degrees of heteroplasmy. cMRI was performed for the six patients with LS carrying MT-ATP6. For Patient 1, imaging was carried out at 16.5 years of age and showed areas of increased T2-signal intensity in the Putamen and Nucleus caudatus on both sides (Figure 6E) and at the perisylvian gray matter (Figure S12H).

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For patient 2, imaging was carried out at 2.2 years of age and showed lesional areas in the Putamen and Nucleus caudatus in both T2-weighted images (Figure 6E) and Fluid Attenuated Inversion Recovery (FLAIR) images (Figure S12H). For patient 3, imaging was carried out at 5 years of age (Figure 6E) and at 14 years of age (Figure S12H). Areas with increased T2-signal intensity at 5 years of age (Figure 6E) had spontaneously resolved at 14 years of age (Figure S12H). In patient 4, FLAIR imaging was performed at 35 years of age and areas of increased signal intensity at the Nuclei caudati on both sides (Figure 6E) and enlargement of the internal and external liquor spaces due to diffused brain atrophy (Figure S12H). For patient 5, imaging was performed at 4.5 months of age and showed T2-weighted images delayed myelination, enlarged external cerebral spinal fluid spaces, and a general frontal brain atrophy (Figure 6E). cMRI was performed for the six patients with LS carrying MT-ATP6. For Patient 1, imaging was carried out at 16.5 years of age and showed areas of increased T2-signal intensity in the Putamen and Nucleus caudatus on both sides (Figure 6E) and at the perisylvian gray matter (Figure S12H). For patient 2, imaging was carried out at 2.2 years of age and showed lesional areas in the Putamen and Nucleus caudatus in both T2-weighted images (Figure 6E) and Fluid Attenuated Inversion Recovery (FLAIR) images (Figure S12H). For patient 3, imaging was carried out at 5 years of age (Figure 6E) and at 14 years of age (Figure S12H). Areas with increased T2-signal intensity at 5 years of age (Figure 6E) had spontaneously resolved at 14 years of age (Figure S12H). In patient 4, FLAIR imaging was performed at 35 years of age and areas of increased signal intensity at the Nuclei caudati on both sides (Figure 6E) and enlargement of the internal and external liquor spaces due to diffused brain atrophy (Figure S12H). For patient 5, imaging was performed at 4.5 months of age and showed T2-weighted images delayed myelination, enlarged external cerebral spinal fluid spaces, and a general frontal brain atrophy (Figure 6E). For patient 6, imaging was performed at 7.5 years of age and showed areas of increased T2-signal intensity in the Putamen, Pallidum, and Nucleus caudatus on both sides (Figure 6E) and in the cortical gray matter (Figure S12H).

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100 μl of the solution was transferred onto a new white wall, white bottom 96-well plate, and luminescence was measured using an EnSight multimode plate reader (Revvity). CellTiter-Glo assay (Promega) was used to determine cell viability based on cellular ATP concentration. NPCs were isolated using Accutase and seeded onto Geltrex-coated 96-well plates at a density of 1.5 x 105 cells/cm2 and incubated in NPC medium overnight at 37 °C and 5 % CO2.

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The day after, NPCs were treated with DMSO, FCCP+AA or sildenafil dilution series in 100 μl and incubated for 16 h at 37 °C and 5 % CO2. 50 μl Cell Titer-Glo reagent solution was added to each well and placed on a plate shaker (1 min, 100 rpm) and incubated at ambient temperature for 10 min to ensure cell lysis.

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For patient 6, imaging was performed at 7.5 years of age and showed areas of increased T2-signal intensity in the Putamen, Pallidum, and Nucleus caudatus on both sides (Figure 6E) and in the cortical gray matter (Figure S12H). CellTiter-Glo assay (Promega) was used to determine cell viability based on cellular ATP concentration. NPCs were isolated using Accutase and seeded onto Geltrex-coated 96-well plates at a density of 1.5 x 105 cells/cm2 and incubated in NPC medium overnight at 37 °C and 5 % CO2. The day after, NPCs were treated with DMSO, FCCP+AA or sildenafil dilution series in 100 μl and incubated for 16 h at 37 °C and 5 % CO2. 50 μl Cell Titer-Glo reagent solution was added to each well and placed on a plate shaker (1 min, 100 rpm) and incubated at ambient temperature for 10 min to ensure cell lysis. 100 μl of the solution was transferred onto a new white wall, white bottom 96-well plate, and luminescence was measured using an EnSight multimode plate reader (Revvity).