#METABOLOMICS WORKBENCH kevin.cho@wustl.edu_20230826_084448 DATATRACK_ID:4250 STUDY_ID:ST002850 ANALYSIS_ID:AN004668 PROJECT_ID:PR001784 VERSION 1 CREATED_ON September 8, 2023, 9:11 am #PROJECT PR:PROJECT_TITLE Bap1 Promotes Osteoclast Function by Metabolic Reprogramming PR:PROJECT_TYPE Untargeted Metabolomics PR:PROJECT_SUMMARY Treatment of osteoporosis most commonly diminishes osteoclast number which PR:PROJECT_SUMMARY suppresses bone formation thus compromising fracture prevention. Bone formation PR:PROJECT_SUMMARY is not suppressed, however, when bone degradation is reduced by retarding PR:PROJECT_SUMMARY osteoclast functional resorptive capacity, rather than differentiation. We find PR:PROJECT_SUMMARY deletion of deubiquitinase, BRCA1-associated protein 1 (Bap1), in myeloid cells PR:PROJECT_SUMMARY (Bap1∆LysM), arrests osteoclast function but not formation. Bap1∆LysM PR:PROJECT_SUMMARY osteoclasts fail to organize their cytoskeleton which is essential for bone PR:PROJECT_SUMMARY degradation. Consequently, bone mass increases in the mutant mice. We find the PR:PROJECT_SUMMARY deubiquitinase activity of Bap1 regulates osteoclast function by metabolic PR:PROJECT_SUMMARY reprogramming. Bap1 deficient osteoclast lineage cells upregulate the cystine PR:PROJECT_SUMMARY transporter, Slc7a11, by enhanced H2Aub occupancy of its promoter. SLC7A11 PR:PROJECT_SUMMARY regulates cellular ROS levels and redirects the mitochondrial metabolites away PR:PROJECT_SUMMARY from the TCA cycle, both of which are necessary for osteoclast function. Thus in PR:PROJECT_SUMMARY osteoclasts, Bap1 appears to regulate epigenetic-metabolic axis and is a PR:PROJECT_SUMMARY potential target to reduce bone degradation while maintaining osteogenesis in PR:PROJECT_SUMMARY osteoporotic patients. PR:INSTITUTE Washington University in St. Louis PR:DEPARTMENT Pathology and Immunology, Medicine, Chemistry PR:LABORATORY Teitelbaum and Patti Laboratories PR:LAST_NAME Cho PR:FIRST_NAME Kevin PR:ADDRESS 1 Brookings Drive, Campus Box 1134, St. Louis, MO, 63130, USA PR:EMAIL kevin.cho@wustl.edu PR:PHONE 314-935-8813 #STUDY ST:STUDY_TITLE Bap1 Promotes Osteoclast Function by Metabolic Reprogramming ST:STUDY_TYPE Untargeted Metabolomics ST:STUDY_SUMMARY Treatment of osteoporosis most commonly diminishes osteoclast number which ST:STUDY_SUMMARY suppresses bone formation thus compromising fracture prevention. Bone formation ST:STUDY_SUMMARY is not suppressed, however, when bone degradation is reduced by retarding ST:STUDY_SUMMARY osteoclast functional resorptive capacity, rather than differentiation. We find ST:STUDY_SUMMARY deletion of deubiquitinase, BRCA1-associated protein 1 (Bap1), in myeloid cells ST:STUDY_SUMMARY (Bap1∆LysM), arrests osteoclast function but not formation. Bap1∆LysM ST:STUDY_SUMMARY osteoclasts fail to organize their cytoskeleton which is essential for bone ST:STUDY_SUMMARY degradation. Consequently, bone mass increases in the mutant mice. We find the ST:STUDY_SUMMARY deubiquitinase activity of Bap1 regulates osteoclast function by metabolic ST:STUDY_SUMMARY reprogramming. Bap1 deficient osteoclast lineage cells upregulate the cystine ST:STUDY_SUMMARY transporter, Slc7a11, by enhanced H2Aub occupancy of its promoter. SLC7A11 ST:STUDY_SUMMARY regulates cellular ROS levels and redirects the mitochondrial metabolites away ST:STUDY_SUMMARY from the TCA cycle, both of which are necessary for osteoclast function. Thus in ST:STUDY_SUMMARY osteoclasts, Bap1 appears to regulate epigenetic-metabolic axis and is a ST:STUDY_SUMMARY potential target to reduce bone degradation while maintaining osteogenesis in ST:STUDY_SUMMARY osteoporotic patients. ST:INSTITUTE Washington University in St. Louis ST:DEPARTMENT Pathology and Immunology, Medicine, Chemistry ST:LABORATORY Teitelbaum and Patti Laboratories ST:LAST_NAME Cho ST:FIRST_NAME Kevin ST:ADDRESS 1 Brookings Drive, Campus Box 1134, St. Louis, MO, 63130, USA ST:EMAIL kevin.cho@wustl.edu ST:PHONE 314-935-8813 #SUBJECT SU:SUBJECT_TYPE Cultured cells SU:SUBJECT_SPECIES Homo sapiens SU:TAXONOMY_ID 9606 #SUBJECT_SAMPLE_FACTORS: SUBJECT(optional)[tab]SAMPLE[tab]FACTORS(NAME:VALUE pairs separated by |)[tab]Raw file names and additional sample data SUBJECT_SAMPLE_FACTORS - Pos_WT_1 Genotype:Wild-type Polarity=Positive; RAW_FILE_NAME=Pos_WT_1.mzML SUBJECT_SAMPLE_FACTORS - Pos_WT_2 Genotype:Wild-type Polarity=Positive; RAW_FILE_NAME=Pos_WT_2.mzML SUBJECT_SAMPLE_FACTORS - Pos_WT_3 Genotype:Wild-type Polarity=Positive; RAW_FILE_NAME=Pos_WT_3.mzML SUBJECT_SAMPLE_FACTORS - Pos_WT_4 Genotype:Wild-type Polarity=Positive; RAW_FILE_NAME=Pos_WT_4.mzML SUBJECT_SAMPLE_FACTORS - Pos_WT_5 Genotype:Wild-type Polarity=Positive; RAW_FILE_NAME=Pos_WT_5.mzML SUBJECT_SAMPLE_FACTORS - Pos_KO_1 Genotype:Knockout Polarity=Positive; RAW_FILE_NAME=Pos_KO_1.mzML SUBJECT_SAMPLE_FACTORS - Pos_KO_2 Genotype:Knockout Polarity=Positive; RAW_FILE_NAME=Pos_KO_2.mzML SUBJECT_SAMPLE_FACTORS - Pos_KO_3 Genotype:Knockout Polarity=Positive; RAW_FILE_NAME=Pos_KO_3.mzML SUBJECT_SAMPLE_FACTORS - Pos_KO_4 Genotype:Knockout Polarity=Positive; RAW_FILE_NAME=Pos_KO_4.mzML SUBJECT_SAMPLE_FACTORS - Pos_KO_5 Genotype:Knockout Polarity=Positive; RAW_FILE_NAME=Pos_KO_5.mzML SUBJECT_SAMPLE_FACTORS - Neg_WT_1 Genotype:Wild-type Polarity=Negative; RAW_FILE_NAME=Neg_WT_1.mzML SUBJECT_SAMPLE_FACTORS - Neg_WT_2 Genotype:Wild-type Polarity=Negative; RAW_FILE_NAME=Neg_WT_2.mzML SUBJECT_SAMPLE_FACTORS - Neg_WT_3 Genotype:Wild-type Polarity=Negative; RAW_FILE_NAME=Neg_WT_3.mzML SUBJECT_SAMPLE_FACTORS - Neg_WT_4 Genotype:Wild-type Polarity=Negative; RAW_FILE_NAME=Neg_WT_4.mzML SUBJECT_SAMPLE_FACTORS - Neg_WT_5 Genotype:Wild-type Polarity=Negative; RAW_FILE_NAME=Neg_WT_5.mzML SUBJECT_SAMPLE_FACTORS - Neg_KO_1 Genotype:Knockout Polarity=Negative; RAW_FILE_NAME=Neg_KO_1.mzML SUBJECT_SAMPLE_FACTORS - Neg_KO_2 Genotype:Knockout Polarity=Negative; RAW_FILE_NAME=Neg_KO_2.mzML SUBJECT_SAMPLE_FACTORS - Neg_KO_3 Genotype:Knockout Polarity=Negative; RAW_FILE_NAME=Neg_KO_3.mzML SUBJECT_SAMPLE_FACTORS - Neg_KO_4 Genotype:Knockout Polarity=Negative; RAW_FILE_NAME=Neg_KO_4.mzML SUBJECT_SAMPLE_FACTORS - Neg_KO_5 Genotype:Knockout Polarity=Negative; RAW_FILE_NAME=Neg_KO_5.mzML #COLLECTION CO:COLLECTION_SUMMARY Primary mus musculus cells CO:SAMPLE_TYPE Osteoclast #TREATMENT TR:TREATMENT_SUMMARY All in vitro experiments were performed at least 3 times. Primary bone marrow TR:TREATMENT_SUMMARY macrophages (BMMs) were prepared as described with slight modification. Marrow TR:TREATMENT_SUMMARY was extracted from femora and tibiae of 6- to 8-week-old mice with α minimum TR:TREATMENT_SUMMARY essential medium (α-MEM) and cultured in α-MEM containing 10% inactivated TR:TREATMENT_SUMMARY fetal bovine serum, 100 IU/mL penicillin, and 100 μg/mL streptomycin (α-10 TR:TREATMENT_SUMMARY medium) with 1:10 of mMCSF producing cell line, CMG 14-12 condition media on TR:TREATMENT_SUMMARY petri-plastic dishes. Cells were incubated at 37°C in 5% CO2 for 3 days and TR:TREATMENT_SUMMARY then washed with phosphate-buffered saline (PBS) and lifted with 1X trypsin/EDTA TR:TREATMENT_SUMMARY in PBS. A total of 1.2 × 104 BMMs were cultured in 500 μL α-MEM containing TR:TREATMENT_SUMMARY 10% heat-inactivated fetal bovine serum with glutathione-S transferase–RANKL TR:TREATMENT_SUMMARY and 30 ng/mL of mouse recombinant macrophage colony-stimulating factor (M-CSF) TR:TREATMENT_SUMMARY in 48-well tissue culture plates, some containing sterile bovine bone slices. #SAMPLEPREP SP:SAMPLEPREP_SUMMARY Cells were quenched with cold LC/MS-grade methanol, then scraped and transferred SP:SAMPLEPREP_SUMMARY to Eppendorf tubes. Samples were dried in a SpeedVac. The samples were then SP:SAMPLEPREP_SUMMARY reconstituted in 1 mL of cold methanol:acetonitrile:water (2:2:1) and subjected SP:SAMPLEPREP_SUMMARY to three cycles of vortexing, freezing in liquid nitrogen, and 10 min of SP:SAMPLEPREP_SUMMARY sonication at 25 °C. Samples were stored at −20 °C overnight and then SP:SAMPLEPREP_SUMMARY centrifuged for 10 min at 14,000×g and 4 °C. Supernatants were transferred to SP:SAMPLEPREP_SUMMARY new tubes and dried by a SpeedVac. The protein abundance of each sample was SP:SAMPLEPREP_SUMMARY determined by using BCA. A quantity of 1 μl of acetonitrile:water (2:1) per SP:SAMPLEPREP_SUMMARY each 2.5 μg of protein was used. Samples were subjected to two cycles of SP:SAMPLEPREP_SUMMARY vortexing and 10 min of sonication at 25 °C. Next, samples were centrifuged for SP:SAMPLEPREP_SUMMARY 10 min at 14,000×g and 4 °C, transferred supernatant to LC vials, and stored SP:SAMPLEPREP_SUMMARY at −80 °C until MS analysis #CHROMATOGRAPHY CH:CHROMATOGRAPHY_TYPE HILIC CH:INSTRUMENT_NAME Thermo Vanquish Flex UHPLC Systems CH:COLUMN_NAME HILICON iHILIC-(P) Classic (100 x 2.1mm,5um) CH:SOLVENT_A 20 mM ammonium bicarbonate, 0.1% ammonium hydroxideand 2.5 μM medronic acid in CH:SOLVENT_A water:acetonitrile (95:5) CH:SOLVENT_B acetonitrile:water (95:5) CH:FLOW_GRADIENT 0–1 min: 90% B, 1–12 min: 90-35% B, 12–12.5 min: 35-25% B, 12.5–14.5 CH:FLOW_GRADIENT min: 25% B CH:FLOW_RATE 250 uL/min CH:COLUMN_TEMPERATURE 45 #ANALYSIS AN:ANALYSIS_TYPE MS #MS MS:INSTRUMENT_NAME Thermo Orbitrap ID-X tribrid MS:INSTRUMENT_TYPE Orbitrap MS:MS_TYPE ESI MS:ION_MODE NEGATIVE MS:MS_COMMENTS Data were collected with the following MS source settings: spray voltage, -2.8 MS:MS_COMMENTS kV; sheath gas, 50; auxiliary gas, 10; sweep gas, 1; ion transfer tube MS:MS_COMMENTS temperature, 300°C; vaporizer temperature, 200°C; mass range, 67 – 1000 Da; MS:MS_COMMENTS resolution, 120,000; maximum injection time, 200 ms; isolation window, 1.5 Da. MS:MS_COMMENTS XCMS and Skyline software were used for data processing MS:MS_RESULTS_FILE ST002850_AN004668_Results.txt UNITS:peak area Has m/z:Yes Has RT:Yes RT units:Seconds #END