#METABOLOMICS WORKBENCH cendalfr_20240411_081443 DATATRACK_ID:4771 STUDY_ID:ST003169 ANALYSIS_ID:AN005201 PROJECT_ID:PR001970 VERSION 1 CREATED_ON April 11, 2024, 8:27 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 - 1 Factor:WT CART in vivo | Sample source:Cells RAW_FILE_NAME(Raw File Name)=1 SUBJECT_SAMPLE_FACTORS - 2 Factor:WT CART in vivo | Sample source:Cells RAW_FILE_NAME(Raw File Name)=2 SUBJECT_SAMPLE_FACTORS - 3 Factor:WT CART in vivo | Sample source:Cells RAW_FILE_NAME(Raw File Name)=3 SUBJECT_SAMPLE_FACTORS - 4 Factor:MCJ KO CART in vivo | Sample source:Cells RAW_FILE_NAME(Raw File Name)=4 SUBJECT_SAMPLE_FACTORS - 5 Factor:MCJ KO CART in vivo | Sample source:Cells RAW_FILE_NAME(Raw File Name)=5 SUBJECT_SAMPLE_FACTORS - 6 Factor:MCJ KO CART in vivo | Sample source:Cells RAW_FILE_NAME(Raw File Name)=6 #COLLECTION CO:COLLECTION_SUMMARY The E2a cells (106) were cultured in CMM for no more than 2 passages before CO:COLLECTION_SUMMARY intravenous tail vail injection to B6 mice 3 days before CAR-T cell injection. CO:COLLECTION_SUMMARY The E2a-bearing mice were irradiated with 500cGy sublethal dosage the day before CO:COLLECTION_SUMMARY CAR-T cell injection. The murine CD8 CAR-T cells were generated and expanded CO:COLLECTION_SUMMARY with rhIL-2 (60 IU/ml) as described above. The expanded CD8 CAR-T cells were CO:COLLECTION_SUMMARY washed with PBS, and 106 CAR+ cells were injected into the E2a-bearing mice via CO:COLLECTION_SUMMARY intravenous tail vail injection. The mice were followed for survival with the CO:COLLECTION_SUMMARY humane end point of development of hind limb paralysis, or weight loss of more CO:COLLECTION_SUMMARY than 20% of the original weight, or signs of major discomfort as determined by CO:COLLECTION_SUMMARY the institutional veterinarian. 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 Positive Ion Mode CH:CHROMATOGRAPHY_TYPE Reversed phase CH:INSTRUMENT_NAME Exploris120 CH:COLUMN_NAME Phenomenex Kinetex C18 (150 x 2.1mm,1.7um) CH:SOLVENT_A 100% water; 0.1% formic acid CH:SOLVENT_B 100% acetonitrile; 0.1% formic acid CH:FLOW_GRADIENT 0-0.5 min 5% B, 0.5-1.1 min 5-95% B, 1.1-2.75 min hold at 95% B, 2.75-3 min CH:FLOW_GRADIENT 95-5% B, 3-5 min hold at 5% 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 POSITIVE 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 1 2 3 4 5 6 Factors Factor:WT CART in vivo | Sample source:Cells Factor:WT CART in vivo | Sample source:Cells Factor:WT CART in vivo | Sample source:Cells Factor:MCJ KO CART in vivo | Sample source:Cells Factor:MCJ KO CART in vivo | Sample source:Cells Factor:MCJ KO CART in vivo | Sample source:Cells L-alanine 1197023.88 1327983.88 1022429.81 1568968.62 1427793.12 1062461 L-arginine 6863230.5 7222230.5 6243684.5 7980496 7930764 6132052.5 L-asparagine 535468.31 476826.5 450014.75 631193.06 505875 375585 L-aspartate 1372252.62 1483275.12 1116382.38 1451198.62 1424129 1146679.62 L-glutamate 3973126.75 3948598.75 3736170 4412249.5 4241764.5 3648352 L-glutamine 8488004 8887393 7065745.5 10065109 9675385 7004350 L-histidine 453154.34 577390.25 269786.47 415080.84 422430 382865.53 L-leucine/L-isoleucine 24789086 27747430 24184186 28680718 26054418 20049822 L-lysine 775457.31 877422.56 377104.09 806658.81 727064.5 675014.25 L-methionine 7392514.5 8478231 7065848 8697247 8380496 6430578.5 L-phenylalanine 6978496.5 8475595 6852887.5 7940340 7643455.5 6032851.5 L-proline 6982688 6567523.5 7047762 7652542.5 7620930.5 6172780 L-serine 427444.22 485046.16 345151.25 514835.25 394962.66 229377.73 L-threonine 485082.16 524086.28 511597.22 528426.88 403367.66 419341.84 L-tryptophan 3562216.75 4013098.75 3605524.75 3124009.75 3073252.75 2051719.88 L-tyrosine 10081315 10097824 9413260 9469005 9446284 8265036 L-valine 5042666.5 5201343.5 4247850.5 5328159.5 5261880 4673793.5 AMP 456886.5 351903.41 297473.53 348723.72 443815.5 500947.84 Adenosine 707023.75 664739.56 720749.81 745050.44 850719.25 1729506 Guanine 323993.69 358170.78 292883.28 359655.97 364053.09 299765.22 CMP 71679.34 66506.85 50993.55 79041.96 74343.79 85925.59 Hypoxanthine 358667.34 377833.62 363256.12 335150.09 354565.38 366094.12 Urate 759133.5 815769.31 771022.94 702023.81 665949.5 692983.06 Nicotinamide 1961781.12 1801942.62 1629010.38 1850226.88 1589012 1885181.5 5-Oxoproline 10309443 12489417 8682290 10292717 11624371 8675300 S-Glutathionyl-L-cysteine 224014.3 296579.34 169744.86 320564.03 339876.75 191665.62 gamma-L-Glutamyl-L-cysteine 184416.39 189766.45 110685.09 78813.71 104129.03 163364.39 Ornithine 180562.64 259328.88 27569.28 77610.2 115839.06 36205.36 L-Citrulline 180369.12 164223.02 203855.31 113525.44 134043.44 139997.25 Creatine 4770057 8793808 4054201 4360741.5 3005996.75 10805841 Creatinine 2846940 3534683.25 2355705 2754858 2667432.25 3342950.75 N-Acetyl-L-citrulline 12353771 13820144 11396885 15381347 12215839 10168484 Guanidinoacetate 117404.18 72310.2 98977.09 56083.73 84498.34 67815.17 Pantothenol 440249.59 518334.91 404414.91 529658.81 479921.66 395565.91 Taurine 1408399.12 1351138.62 821823.5 1320948.75 1256985.25 1125754.62 Indole-3-acetaldehyde 285553.47 277493.47 263842.72 8207.73 5372.33 25682.28 Indole-3-acetate 1448145.5 1526587.38 1911843.12 1680266.88 1729845.5 1299315.88 6-Hydroxykynurenic acid 1486375.88 1398272.62 1111398 737258.19 744064.31 398366.47 kynurenine 23525.04 34734.91 31615.96 68574 65982.12 42198.25 N-formyl kynurenine 7078.12 5688.14 8759.02 36287.55 37959.28 22354.58 Anthranilate 230236.42 208531.12 234244.56 180784.58 203353.31 150428.47 g-Oxalo-crotonate 124694.13 104803.19 104126.43 135527.92 135116.95 78721.22 2-Oxoadipate 123582.88 135552.73 192910.25 185970.05 162221.08 104098.6 L-Adrenaline 215566 391056.41 542457.81 226354.56 263924.34 458769.59 Ethanolamine phosphate 337839.84 338737.34 214072.86 291651.41 360397.53 314050.91 Sphingosine 631332.44 368950.78 351429.72 546680.56 492058.91 650668.81 Acetylcholine 139253.92 115964.66 184844.95 113749.4 213390.48 370313.41 Choline 10643782 11372032 12102527 10968815 11590809 10520196 L-Carnitine 4897933.5 5952352.5 3980325.25 4253042.5 3873179.25 6830796 acyl-C2 (acetyl-carnitine) 4928999.5 5844600 3997628 4427018.5 5025709.5 5826114.5 acyl-C3 (propionyl-carnitine) 404599.66 445941.59 396862.59 369899.28 389751.72 449780.78 acyl-C4 (butanoyl-l-carnitine) 144729.33 152380.14 132910.02 127478.52 166861.56 101832.57 acyl-C4-OH (Hydroxybutyrylcarnitine) 194528.62 234728.06 143606.22 179798.36 199170.86 222721.3 acyl-C4-DC 22472.05 40887.15 17242.7 27167.21 27819.52 50310.48 acyl-C6 (hexanoyl-l-carnitine) 78703.78 68030.15 64582.07 74810.56 57538.34 75826.67 acyl-C14 (O-tetradecanoyl-L-carnitine) 474356.84 60020.62 18004.3 152064.39 235384.45 44302.54 acyl-C18 (Octadecanoyl-L-carnitine) 4398604.5 539934.06 98986.34 1182649.38 1317746.25 566479.94 acyl-C20 947354.69 1089732.12 851443.69 692495.62 740909.75 695332.75 acyl-C20:4 288275.88 595105.12 273191.84 126742.95 218085.8 130637.21 MS_METABOLITE_DATA_END #METABOLITES METABOLITES_START metabolite_name CmpdID parent medRt L-alanine C00041 90.055092 0.656 L-arginine C00062 175.118912 0.637 L-asparagine C00152 133.060074 0.661 L-aspartate C00049 134.044876 0.671 L-glutamate C00025 148.060455 0.667 L-glutamine C00064 147.076462 0.664 L-histidine C00135 156.076797 0.63 L-leucine/L-isoleucine C00123 132.102005 1.005 L-lysine C00047 147.112869 0.636 L-methionine C00073 150.058319 0.895 L-phenylalanine C00079 166.086288 1.416 L-proline C00148 116.070793 0.689 L-serine C00065 106.050072 0.659 L-threonine C00188 120.065681 0.662 L-tryptophan C00078 205.097153 1.761 L-tyrosine C00082 182.081131 0.899 L-valine C00183 118.086433 0.668 AMP C00020 348.070404 0.741 Adenosine C00212 268.104034 0.895 Guanine C00242 152.05452 0.897 CMP C00055 324.059174 0.685 Hypoxanthine C00262 137.045883 0.883 Urate C00366 169.035522 0.894 Nicotinamide C00153 123.055458 0.904 5-Oxoproline C01879 130.049942 0.943 S-Glutathionyl-L-cysteine C05526 427.095123 0.675 gamma-L-Glutamyl-L-cysteine C00669 251.069855 0.895 Ornithine C01602 133.09726 0.627 L-Citrulline C00327 176.102966 0.669 Creatine C00300 132.076859 0.674 Creatinine C00791 114.066383 0.734 N-Acetyl-L-citrulline C15532 218.113541 0.661 Guanidinoacetate C00581 118.061272 0.674 Pantothenol C00864 220.117981 1.711 Taurine C00245 126.022072 0.666 Indole-3-acetaldehyde C00637 160.075653 1.133 Indole-3-acetate C00954 176.07074 1.969 6-Hydroxykynurenic acid C08480 206.048141 0.904 kynurenine C00328 209.091934 1.421 N-formyl kynurenine C02700 237.087021 1.051 Anthranilate C00108 138.055038 1.8 g-Oxalo-crotonate C03453 159.027679 0.888 2-Oxoadipate C00322 161.046036 1.97 L-Adrenaline C00788 184.095642 0.662 Ethanolamine phosphate C00346 142.026413 0.662 Sphingosine C00319 300.289764 2.149 Acetylcholine C01996 146.117569 0.739 Choline C00114 104.107201 0.652 L-Carnitine C00318 162.112473 0.666 acyl-C2 (acetyl-carnitine) C02571 204.123032 0.886 acyl-C3 (propionyl-carnitine) C03017 218.138626 1.061 acyl-C4 (butanoyl-l-carnitine) C02862 232.154358 1.75 acyl-C4-OH (Hydroxybutyrylcarnitine) HMDB13127 248.149384 0.897 acyl-C4-DC HMDB13133 262.128693 0.893 acyl-C6 (hexanoyl-l-carnitine) HMDB00756 260.185669 1.824 acyl-C14 (O-tetradecanoyl-L-carnitine) HMDB05066 372.311218 2.05 acyl-C18 (Octadecanoyl-L-carnitine) HMDB00848 428.373535 2.624 acyl-C20 ac124 458.417389 0.6 acyl-C20:4 ac125 448.341461 2.642 METABOLITES_END #END