#METABOLOMICS WORKBENCH cendalfr_20240411_082827 DATATRACK_ID:4772 STUDY_ID:ST003170 ANALYSIS_ID:AN005202 PROJECT_ID:PR001970 VERSION 1 CREATED_ON April 11, 2024, 8:36 am #PROJECT PR:PROJECT_TITLE Releasing the mitochondrial respiration brake MCJ/DnaJC15 enhances CD8 CAR-T PR:PROJECT_TITLE cell therapy efficacy PR:PROJECT_SUMMARY Metabolism of chimeric antigen receptor (CAR) T cells is emerging as an PR:PROJECT_SUMMARY important area to improve CAR-T cell therapy in cancer treatment. Mitochondrial PR:PROJECT_SUMMARY respiration is essential for survival and function of CAR-T cells, but PR:PROJECT_SUMMARY developing strategies to specifically enhance mitochondrial respiration has been PR:PROJECT_SUMMARY challenging. Here we identify MCJ/DnaJC15, an endogenous negative regulator of PR:PROJECT_SUMMARY mitochondrial Complex I, as a metabolic target to enhance mitochondrial PR:PROJECT_SUMMARY respiration in CD8 CAR-T cells. Loss of MCJ in CD8 CAR-T cells increases their PR:PROJECT_SUMMARY in vitro and in vivo efficacy against mouse B cell leukemias. MCJ deficiency in PR:PROJECT_SUMMARY TCR- specific CD8 cells also increases their efficacy against solid tumors in PR:PROJECT_SUMMARY vivo. Furthermore, we reveal that human CD8 cells express MCJ and that silencing PR:PROJECT_SUMMARY MCJ expression increases mitochondrial metabolism and anti-tumor activity of PR:PROJECT_SUMMARY human CAR-T cells. Thus, targeting MCJ to enhance mitochondrial metabolism is a PR:PROJECT_SUMMARY promising therapeutic strategy to improve the efficacy of adoptive T cell PR:PROJECT_SUMMARY therapies. PR:INSTITUTE University of Colorado School of Medicine PR:LABORATORY Laboratory of Angelo D'Alessandro in collaboration with Mercedes Rincon PR:LAST_NAME Cendali PR:FIRST_NAME Francesca PR:ADDRESS 13199 East Montview Boulevard, Aurora, CO, 80045, USA PR:EMAIL francesca.cendali@cuanschutz.edu PR:PHONE 3037246131 #STUDY ST:STUDY_TITLE Releasing the mitochondrial respiration brake MCJ/DnaJC15 enhances CD8 CAR-T ST:STUDY_TITLE cell therapy efficacy ST:STUDY_SUMMARY Metabolism of chimeric antigen receptor (CAR) T cells is emerging as an ST:STUDY_SUMMARY important area to improve CAR-T cell therapy in cancer treatment. Mitochondrial ST:STUDY_SUMMARY respiration is essential for survival and function of CAR-T cells, but ST:STUDY_SUMMARY developing strategies to specifically enhance mitochondrial respiration has been ST:STUDY_SUMMARY challenging. Here we identify MCJ/DnaJC15, an endogenous negative regulator of ST:STUDY_SUMMARY mitochondrial Complex I, as a metabolic target to enhance mitochondrial ST:STUDY_SUMMARY respiration in CD8 CAR-T cells. Loss of MCJ in CD8 CAR-T cells increases their ST:STUDY_SUMMARY in vitro and in vivo efficacy against mouse B cell leukemias. MCJ deficiency in ST:STUDY_SUMMARY TCR- specific CD8 cells also increases their efficacy against solid tumors in ST:STUDY_SUMMARY vivo. Furthermore, we reveal that human CD8 cells express MCJ and that silencing ST:STUDY_SUMMARY MCJ expression increases mitochondrial metabolism and anti-tumor activity of ST:STUDY_SUMMARY human CAR-T cells. Thus, targeting MCJ to enhance mitochondrial metabolism is a ST:STUDY_SUMMARY promising therapeutic strategy to improve the efficacy of adoptive T cell ST:STUDY_SUMMARY therapies. ST:INSTITUTE University of Colorado School of Medicine ST:LABORATORY Laboratory of Angelo D'Alessandro in collaboration with Mercedes Rincon ST:LAST_NAME Cendali ST:FIRST_NAME Francesca ST:ADDRESS 13199 East Montview Boulevard, Aurora, CO, 80045, USA ST:EMAIL francesca.cendali@cuanschutz.edu ST:PHONE 3037246131 #SUBJECT SU:SUBJECT_TYPE Cultured cells SU:SUBJECT_SPECIES Mus musculus #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 - A Factor:WT CART med | Sample source:Cells RAW_FILE_NAME(Raw File Name)=1 SUBJECT_SAMPLE_FACTORS - B Factor:WT CART med | Sample source:Cells RAW_FILE_NAME(Raw File Name)=2 SUBJECT_SAMPLE_FACTORS - C Factor:WT CART med | Sample source:Cells RAW_FILE_NAME(Raw File Name)=3 SUBJECT_SAMPLE_FACTORS - D Factor:MCJ KO CART med | Sample source:Cells RAW_FILE_NAME(Raw File Name)=4 SUBJECT_SAMPLE_FACTORS - E Factor:MCJ KO CART med | Sample source:Cells RAW_FILE_NAME(Raw File Name)=5 SUBJECT_SAMPLE_FACTORS - F Factor:MCJ KO CART med | Sample source:Cells RAW_FILE_NAME(Raw File Name)=6 #COLLECTION CO:COLLECTION_SUMMARY Murine CD8 cells were isolated from lymph nodes and spleen using negative CO:COLLECTION_SUMMARY selection with CD8+ T cell isolation kit (for generation of CAR-T cells) CO:COLLECTION_SUMMARY (Miltenyi, order# 130-104-075) or positive selection (for OT-I CD8 cells) with CO:COLLECTION_SUMMARY CD8 (Ly-2) Microbeads (Miltenyi, order# 130-117-044). Mouse CD8 cells were CO:COLLECTION_SUMMARY activated with plate-bound anti-CD3 (5 g/ml) and soluble anti-CD28 mAbs (1 CO:COLLECTION_SUMMARY g/ml) for 48h for WT and cMCJ KO CD8 studies and OT-I CD8 cells studies. CO:SAMPLE_TYPE T-cells #TREATMENT TR:TREATMENT_SUMMARY Metabolomics differences in this experiment are observed at baseline #SAMPLEPREP SP:SAMPLEPREP_SUMMARY CAR-T cells were isolated as described above either from in vitro culture or SP:SAMPLEPREP_SUMMARY from bone marrow harvested in an in vivo study. The cells were washed in PBS and SP:SAMPLEPREP_SUMMARY frozen at -80C until the assay is ready to run. Metabolites from cells were SP:SAMPLEPREP_SUMMARY extracted at 2x106 cells/ml at 4°C (30 min) in the presence of 5:3:2 SP:SAMPLEPREP_SUMMARY MeOH:MeCN:water (v/v/v). The samples were spun down and the resulting SP:SAMPLEPREP_SUMMARY supernatant was transferred to new tubes and dried under a vacuum. The resulting SP:SAMPLEPREP_SUMMARY residue was reconstituted in 0.1% formic acid at a 3x concentration, then SP:SAMPLEPREP_SUMMARY analyzed on a Thermo Vanquish UHPLC coupled to a Thermo Q Exactive MS as SP:SAMPLEPREP_SUMMARY previously described in detail. #CHROMATOGRAPHY CH:CHROMATOGRAPHY_SUMMARY Negative ion Mode CH:CHROMATOGRAPHY_TYPE Reversed phase CH:INSTRUMENT_NAME Thermo Vanquish CH:COLUMN_NAME Phenomenex Kinetex C18 (150 x 2.1mm,1.7um) CH:SOLVENT_A 95% water/5% acetonitrile; 1 mM ammonium acetate CH:SOLVENT_B 95% acetonitrile/5% water; 1 mM ammonium acetate CH:FLOW_GRADIENT 0-0.5 min 0% B, 0.5-1.1 min 0-100% B, 1.1-2.75 min hold at 100% B, 2.75-3 min CH:FLOW_GRADIENT 100-0% B, 3-5 min hold at 0% B CH:FLOW_RATE 0.450ml/min CH:COLUMN_TEMPERATURE 45 #ANALYSIS AN:ANALYSIS_TYPE MS #MS MS:INSTRUMENT_NAME Thermo Q Exactive Orbitrap MS:INSTRUMENT_TYPE Orbitrap MS:MS_TYPE ESI MS:ION_MODE NEGATIVE MS:MS_COMMENTS Resolution 70,000, scan range 65-900 m/z, maximum injection time 200 ms, MS:MS_COMMENTS microscans 2, automatic gain control (AGC) 3 x 10^6 ions, source voltage 4.0 kV, MS:MS_COMMENTS capillary temperature 320 C, and sheath gas 45, auxiliary gas 15, and sweep gas MS:MS_COMMENTS 0 (all nitrogen). Data converted to mzXML using RawConverter. Metabolites were MS:MS_COMMENTS annotated and integrated using Maven in conjunction with the KEGG database. #MS_METABOLITE_DATA MS_METABOLITE_DATA:UNITS Peak Areas MS_METABOLITE_DATA_START Samples A B C D E F Factors Factor:WT CART med | Sample source:Cells Factor:WT CART med | Sample source:Cells Factor:WT CART med | Sample source:Cells Factor:MCJ KO CART med | Sample source:Cells Factor:MCJ KO CART med | Sample source:Cells Factor:MCJ KO CART med | Sample source:Cells ATP 139159.47 170913.86 196101.25 229624.38 239588.77 212123.92 ADP 460100.28 321440.47 347160.09 561973.19 514727.5 558519.12 AMP 14696773 7411730.5 5901511.5 11825073 9307989 12111243 Guanosine 706371.5 583870.81 772630.19 651877.94 751452.19 1000826.25 Guanine 179010.77 192137.44 212885.33 199917.88 172953.22 211659.38 CTP 163354.23 155117.89 185706.33 214626.2 217024.14 255378.45 Inosine 1401242.12 1117825.62 1240428.38 1018568 1246078.12 1501443.12 Urate 2538730.25 910437.75 1245977.62 3304054 3013126 2129854.75 4-Pyridoxate 240387.02 124630.84 140313.17 264367.44 261100 278331.44 UDP-glucose 882831 1013224.5 1020436.5 1282072.5 1601022.62 952133.5 ADP-D-ribose 185038.61 112892.6 72200.15 83368.65 182623.33 162172.62 Flavin mononucleotide 136271.92 17141.96 55133.75 112020.66 119061.91 74165.75 Phosphate 87673848 86956008 94770056 69843016 79346256 85205240 Diphosphate 12571133 11159006 14998676 10029219 10777273 13078604 D-Glucose 1568506.62 1332253.5 1374051.12 1570285.62 1461848 1840128.88 D-Glyceraldehyde 3-phosphate/Glycerone phosphate 22737178 22080746 22010212 20847602 25759560 23411942 2/3-Phospho-D-glycerate 126825.31 36065.2 93441.79 80811.48 86920.93 134233.8 Pyruvate 1467146.38 753187.81 945885.25 2028017.62 1978371.12 1504044.5 Lactate 151183952 46993744 58135148 193258832 188688720 113521112 Maltose 163767.16 42327.64 68252.37 151615.56 156826.39 129142.88 Mannitol 973521.31 653739.44 836902.19 1196732.75 1001202.5 1060230.38 Citrate 1721370 514696.38 3115143 1689266.62 1185861.12 1532289.62 2-Oxoglutarate 196121.5 234366.7 323343.34 390385 368754.5 291902.72 Succinate 2060473.5 2083517 1757345.38 2301849.75 2229485.5 2361560.25 Fumarate 128623.55 71427.29 99814.27 191135.31 158932.5 121122.19 Malate 737415.69 313349.91 361115.84 787071.69 639734.5 638931.81 2-Hydroxyglutarate/Citramalate 649850.31 785034.5 807255.19 680504.25 822936.19 823706.31 Sedoheptulose 1-phosphate 1972689 2490104.75 2329230 2553944 2259548.75 2353439.25 alpha-D-Ribose 1-phosphate 303227.47 249294.44 247072.89 236807.62 247983 356669.84 Glutathione 39433228 36647368 36258580 50548148 53291796 52519536 S-Glutathionyl-L-cysteine 94909.62 110609.29 75721.62 115246.91 108462.25 141789.06 Dimethylglycine 270290.47 270398.66 268578.41 409909.16 403506.5 314898 N-Glycoloyl-neuraminate 4042426.25 4234706.5 4458959.5 6135506 4862716.5 4595501.5 UDP-N-acetyl-D-glucosamine 2857343.75 2416663.25 2524671 2507129.75 3704986.25 3425814.25 Phosphocreatine 190679.58 170025.55 183980 213917.77 208065.8 242989.69 N-Acetylornithine 84561.62 26509.86 36828.94 133748.45 131251.31 72074.24 Thiocysteine 33037.57 15142.17 43580.02 29794.14 28565.74 31926.61 Hexanoic acid (caproate) 951465 950341.44 1049168.88 1627820.62 1024610.56 1070548.62 Heptanoic acid 1187286.88 1200581.5 1390521.12 1891618.88 1512472.5 1342461.25 Octanoic acid (caprylate) 4484996 3851951.25 4811065.5 4691206.5 4378506.5 4653606.5 Nonanoic acid (pelargonate) 40871824 36044604 44527328 49873996 45871040 44914516 Decanoic acid (caprate) 18006338 16170040 16942330 15709861 19278966 22214190 Dodecanoic acid 11174421 11574391 10899474 10029879 12469247 11884756 Tetradecanoic acid 44788820 33189776 27799504 22755806 25780560 27756518 Hexadecanoic acid 148489632 113073344 115519552 77453728 78738520 93553928 Octadecanoic acid 2893985.25 3862629.25 3347352 3827461.75 3493608 3525607.75 Tetradecenoic acid 5203684.5 4409807.5 4073754.75 2057463 4869235 6195874.5 Hexadecenoic acid 54337036 42065228 33676548 18411496 22010606 31767574 Octadecenoic acid 38579036 26507568 19933766 11689092 15306057 22154814 Linoleate 8832487 5024178.5 4069594.75 1914747.12 2687335.25 3741257.25 Octadecatrienoic acid 539004.44 333771.31 233257.62 141170.89 223334.75 289780.53 Eicosatetraenoic acid 4374010.5 4493328.5 3179815 1033871.31 1690289.88 2761457.75 Docosahexaenoic acid 1147833.5 1244295.75 728014.94 429859 501239.34 826818.31 (8Z-11Z-14Z)-Icosatrienoic acid 927394.75 968999.56 617018.06 218943.58 374989.16 521112.16 (7Z-10Z-13Z-16Z-19Z)-Docosa-7-10-13-16-19-pentaenoic acid 1314551 1110387.25 771789.75 265715.78 413021.62 695086.94 MS_METABOLITE_DATA_END #METABOLITES METABOLITES_START metabolite_name CmpdID parent medRt ATP C00002 505.989 1.413 ADP C00008 426.022 1.291 AMP C00020 346.056 0.968 Guanosine C00387 282.084 1.070 Guanine C00242 150.041 0.920 CTP C00063 481.978 0.610 Inosine C00294 267.073 1.065 Urate C00366 167.022 0.878 4-Pyridoxate C00847 182.044 0.703 UDP-glucose C00029 565.048 0.815 ADP-D-ribose C01882 558.064 0.816 Flavin mononucleotide C00061 455.102 0.705 Phosphate C00009 96.970 0.607 Diphosphate C00013 176.935 0.828 D-Glucose C00031 179.056 0.684 D-Glyceraldehyde 3-phosphate/Glycerone phosphate C00118 168.989 1.822 2/3-Phospho-D-glycerate C00631 184.985 0.632 Pyruvate C00022 87.009 0.764 Lactate C01432 89.024 0.800 Maltose C00208 341.109 0.708 Mannitol C00392 181.070 0.928 Citrate C00158 191.020 0.628 2-Oxoglutarate C00026 145.014 0.739 Succinate C00042 117.019 0.808 Fumarate C00122 115.004 0.613 Malate C00149 133.014 0.785 2-Hydroxyglutarate/Citramalate C02630 147.030 0.919 Sedoheptulose 1-phosphate C06222 289.033 0.633 alpha-D-Ribose 1-phosphate C00620 229.012 0.639 Glutathione C00051 306.078 0.795 S-Glutathionyl-L-cysteine C05526 425.081 0.633 Dimethylglycine C01026 102.056 0.621 N-Glycoloyl-neuraminate C03410 324.094 0.642 UDP-N-acetyl-D-glucosamine C00043 606.074 0.788 Phosphocreatine C02305 210.029 0.601 N-Acetylornithine C00437 173.093 0.915 Thiocysteine C01962 151.986 0.785 Hexanoic acid (caproate) C01585 115.076 1.938 Heptanoic acid C17714 129.092 2.042 Octanoic acid (caprylate) C06423 143.108 2.136 Nonanoic acid (pelargonate) C01601 157.123 2.219 Decanoic acid (caprate) C01571 171.139 2.302 Dodecanoic acid C02679 199.170 2.497 Tetradecanoic acid C06424 227.202 2.765 Hexadecanoic acid C00249 255.233 3.169 Octadecanoic acid C01530 283.264 2.168 Tetradecenoic acid C08322 225.186 2.550 Hexadecenoic acid C08362 253.217 2.831 Octadecenoic acid C00712 281.249 3.219 Linoleate C01595 279.233 2.929 Octadecatrienoic acid C06427 277.217 2.669 Eicosatetraenoic acid C00219 303.233 2.767 Docosahexaenoic acid C06429 327.233 2.668 (8Z-11Z-14Z)-Icosatrienoic acid C03242 305.249 2.930 (7Z-10Z-13Z-16Z-19Z)-Docosa-7-10-13-16-19-pentaenoic acid C16513 329.249 2.795 METABOLITES_END #END