Metabolomics - Research Accomplishments

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In the 2018 – 2022 period the MSR SR supported approximately 240 publications, of which 50 in high-Impact Factor Journals. The MSR’s high Impact Factor publications are shown below:

 

Zhang Z, TeSlaa T, Xu X, Zeng X, Yang L, Xing G, Tesz GJ, Clasquin MF, Rabinowitz JD. Serine catabolism generates liver NADPH and supports hepatic lipogenesis. Nat Metab. 2021;3(12):1608-20. doi: 10.1038/s42255-021-00487-4. PubMed PMID: 34845393; PMCID: PMC8721747.

Jang C, Chen L, Rabinowitz JD. Metabolomics and Isotope Tracing. Cell. 2018;173(4):822-37. doi: 10.1016/j.cell.2018.03.055. PubMed PMID: 29727671; PMCID: PMC6034115.

Chen L, Lu W, Wang L, Xing X, Chen Z, Teng X, Zeng X, Muscarella AD, Shen Y, Cowan A, McReynolds MR, Kennedy BJ, Lato AM, Campagna SR, Singh M, Rabinowitz JD. Metabolite discovery through global annotation of untargeted metabolomics data. Nat Methods. 2021;18(11):1377-85. doi: 10.1038/s41592-021-01303-3. PubMed PMID: 34711973; PMCID: PMC8733904.

Chen L, Vasoya RP, Toke NH, Parthasarathy A, Luo S, Chiles E, Flores J, Gao N, Bonder EM, Su X, Verzi MP. HNF4 Regulates Fatty Acid Oxidation and Is Required for Renewal of Intestinal Stem Cells in Mice. Gastroenterology. 2020;158(4):985-99.e9. doi: 10.1053/j.gastro.2019.11.031. PubMed PMID: 31759926; PMCID: PMC7062567.

Liu J, Zhang C, Wu H, Sun XX, Li Y, Huang S, Yue X, Lu SE, Shen Z, Su X, White E, Haffty BG, Hu W, Feng Z. Parkin ubiquitinates phosphoglycerate dehydrogenase to suppress serine synthesis and tumor progression. J Clin Invest. 2020;130(6):3253-69. doi: 10.1172/jci132876. PubMed PMID: 32478681; PMCID: PMC7260041.

Poillet-Perez L, Xie X, Zhan L, Yang Y, Sharp DW, Hu ZS, Su X, Maganti A, Jiang C, Lu W, Zheng H, Bosenberg MW, Mehnert JM, Guo JY, Lattime E, Rabinowitz JD, White E. Autophagy maintains tumour growth through circulating arginine. Nature. 2018;563(7732):569-73. doi: 10.1038/s41586-018-0697-7. PubMed PMID: 30429607; PMCID: PMC6287937.

Zhang H, Su X, Burley SK, Zheng XFS. mTOR regulates aerobic glycolysis through NEAT1 and nuclear paraspeckle-mediated mechanism in hepatocellular carcinoma. Theranostics. 2022;12(7):3518-33. doi: 10.7150/thno.72581. PubMed PMID: 35547764; PMCID: PMC9065186.

Yang L, TeSlaa T, Ng S, Nofal M, Wang L, Lan T, Zeng X, Cowan A, McBride M, Lu W, Davidson S, Liang G, Oh TG, Downes M, Evans R, Von Hoff D, Guo JY, Han H, Rabinowitz JD. Ketogenic diet and chemotherapy combine to disrupt pancreatic cancer metabolism and growth. Med (N Y). 2022;3(2):119-36. doi: 10.1016/j.medj.2021.12.008. PubMed PMID: 35425930; PMCID: PMC9004683.

Wang L, Xing X, Zeng X, Jackson SR, TeSlaa T, Al-Dalahmah O, Samarah LZ, Goodwin K, Yang L, McReynolds MR, Li X, Wolff JJ, Rabinowitz JD, Davidson SM. Spatially resolved isotope tracing reveals tissue metabolic activity. Nat Methods. 2022;19(2):223-30. doi: 10.1038/s41592-021-01378-y. PubMed PMID: 35132243.

da Silva-Diz V, Cao B, Lancho O, Chiles E, Alasadi A, Aleksandrova M, Luo S, Singh A, Tao H, Augeri D, Minuzzo S, Indraccolo S, Khiabanian H, Su X, Jin S, Herranz D. A novel and highly effective mitochondrial uncoupling drug in T-cell leukemia. Blood. 2021;138(15):1317-30. doi: 10.1182/blood.2020008955. PubMed PMID: 33876224; PMCID: PMC8525334.

Liu L, Su X, Quinn WJ, 3rd, Hui S, Krukenberg K, Frederick DW, Redpath P, Zhan L, Chellappa K, White E, Migaud M, Mitchison TJ, Baur JA, Rabinowitz JD. Quantitative Analysis of NAD Synthesis-Breakdown Fluxes. Cell Metab. 2018;27(5):1067-80.e5. doi: 10.1016/j.cmet.2018.03.018. PubMed PMID: 29685734; PMCID: PMC5932087.

Lanaspa MA, Andres-Hernando A, Orlicky DJ, Cicerchi C, Jang C, Li N, Milagres T, Kuwabara M, Wempe MF, Rabinowitz JD, Johnson RJ, Tolan DR. Ketohexokinase C blockade ameliorates fructose-induced metabolic dysfunction in fructose-sensitive mice. J Clin Invest. 2018;128(6):2226-38. doi: 10.1172/jci94427. PubMed PMID: 29533924; PMCID: PMC5983342.

Morscher RJ, Ducker GS, Li SH, Mayer JA, Gitai Z, Sperl W, Rabinowitz JD. Mitochondrial translation requires folate-dependent tRNA methylation. Nature. 2018;554(7690):128-32. doi: 10.1038/nature25460. PubMed PMID: 29364879; PMCID: PMC6020024.

Jang C, Hui S, Lu W, Cowan AJ, Morscher RJ, Lee G, Liu W, Tesz GJ, Birnbaum MJ, Rabinowitz JD. The Small Intestine Converts Dietary Fructose into Glucose and Organic Acids. Cell Metab. 2018;27(2):351-61.e3. doi: 10.1016/j.cmet.2017.12.016. PubMed PMID: 29414685; PMCID: PMC6032988.

Ron-Harel N, Notarangelo G, Ghergurovich JM, Paulo JA, Sage PT, Santos D, Satterstrom FK, Gygi SP, Rabinowitz JD, Sharpe AH, Haigis MC. Defective respiration and one-carbon metabolism contribute to impaired naïve T cell activation in aged mice. Proc Natl Acad Sci U S A. 2018;115(52):13347-52. doi: 10.1073/pnas.1804149115. PubMed PMID: 30530686; PMCID: PMC6310842.

Bhatt V, Khayati K, Hu ZS, Lee A, Kamran W, Su X, Guo JY. Autophagy modulates lipid metabolism to maintain metabolic flexibility for Lkb1-deficient Kras-driven lung tumorigenesis. Genes Dev. 2019;33(3-4):150-65. doi: 10.1101/gad.320481.118. PubMed PMID: 30692209; PMCID: PMC6362813.

Neinast MD, Jang C, Hui S, Murashige DS, Chu Q, Morscher RJ, Li X, Zhan L, White E, Anthony TG, Rabinowitz JD, Arany Z. Quantitative Analysis of the Whole-Body Metabolic Fate of Branched-Chain Amino Acids. Cell Metab. 2019;29(2):417-29.e4. doi: 10.1016/j.cmet.2018.10.013. PubMed PMID: 30449684; PMCID: PMC6365191.

Rodriguez AE, Ducker GS, Billingham LK, Martinez CA, Mainolfi N, Suri V, Friedman A, Manfredi MG, Weinberg SE, Rabinowitz JD, Chandel NS. Serine Metabolism Supports Macrophage IL-1β Production. Cell Metab. 2019;29(4):1003-11.e4. doi: 10.1016/j.cmet.2019.01.014. PubMed PMID: 30773464; PMCID: PMC6447453.

Estrella MA, Du J, Chen L, Rath S, Prangley E, Chitrakar A, Aoki T, Schedl P, Rabinowitz J, Korennykh A. The metabolites NADP(+) and NADPH are the targets of the circadian protein Nocturnin (Curled). Nat Commun. 2019;10(1):2367. doi: 10.1038/s41467-019-10125-z. PubMed PMID: 31147539; PMCID: PMC6542800.

Jang C, Hui S, Zeng X, Cowan AJ, Wang L, Chen L, Morscher RJ, Reyes J, Frezza C, Hwang HY, Imai A, Saito Y, Okamoto K, Vaspoli C, Kasprenski L, Zsido GA, 2nd, Gorman JH, 3rd, Gorman RC, Rabinowitz JD. Metabolite Exchange between Mammalian Organs Quantified in Pigs. Cell Metab. 2019;30(3):594-606.e3. doi: 10.1016/j.cmet.2019.06.002. PubMed PMID: 31257152; PMCID: PMC6726553.

Minhas PS, Liu L, Moon PK, Joshi AU, Dove C, Mhatre S, Contrepois K, Wang Q, Lee BA, Coronado M, Bernstein D, Snyder MP, Migaud M, Majeti R, Mochly-Rosen D, Rabinowitz JD, Andreasson KI. Macrophage de novo NAD(+) synthesis specifies immune function in aging and inflammation. Nat Immunol. 2019;20(1):50-63. doi: 10.1038/s41590-018-0255-3. PubMed PMID: 30478397; PMCID: PMC6768398.

Wang W, Ishibashi J, Trefely S, Shao M, Cowan AJ, Sakers A, Lim HW, O'Connor S, Doan MT, Cohen P, Baur JA, King MT, Veech RL, Won KJ, Rabinowitz JD, Snyder NW, Gupta RK, Seale P. A PRDM16-Driven Metabolic Signal from Adipocytes Regulates Precursor Cell Fate. Cell Metab. 2019;30(1):174-89.e5. doi: 10.1016/j.cmet.2019.05.005. PubMed PMID: 31155495; PMCID: PMC6836679.

Benson KK, Hu W, Weller AH, Bennett AH, Chen ER, Khetarpal SA, Yoshino S, Bone WP, Wang L, Rabinowitz JD, Voight BF, Soccio RE. Natural human genetic variation determines basal and inducible expression of PM20D1, an obesity-associated gene. Proc Natl Acad Sci U S A. 2019;116(46):23232-42. doi: 10.1073/pnas.1913199116. PubMed PMID: 31659023; PMCID: PMC6859347.

Stine RR, Sakers AP, TeSlaa T, Kissig M, Stine ZE, Kwon CW, Cheng L, Lim HW, Kaestner KH, Rabinowitz JD, Seale P. PRDM16 Maintains Homeostasis of the Intestinal Epithelium by Controlling Region-Specific Metabolism. Cell Stem Cell. 2019;25(6):830-45.e8. doi: 10.1016/j.stem.2019.08.017. PubMed PMID: 31564549; PMCID: PMC6898778.

Bailis W, Shyer JA, Zhao J, Canaveras JCG, Al Khazal FJ, Qu R, Steach HR, Bielecki P, Khan O, Jackson R, Kluger Y, Maher LJ, 3rd, Rabinowitz J, Craft J, Flavell RA. Distinct modes of mitochondrial metabolism uncouple T cell differentiation and function. Nature. 2019;571(7765):403-7. doi: 10.1038/s41586-019-1311-3. PubMed PMID: 31217581; PMCID: PMC6939459.

Hermans D, Gautam S, García-Cañaveras JC, Gromer D, Mitra S, Spolski R, Li P, Christensen S, Nguyen R, Lin JX, Oh J, Du N, Veenbergen S, Fioravanti J, Ebina-Shibuya R, Bleck C, Neckers LM, Rabinowitz JD, Gattinoni L, Leonard WJ. Lactate dehydrogenase inhibition synergizes with IL-21 to promote CD8(+) T cell stemness and antitumor immunity. Proc Natl Acad Sci U S A. 2020;117(11):6047-55. doi: 10.1073/pnas.1920413117. PubMed PMID: 32123114; PMCID: PMC7084161.

Ghergurovich JM, García-Cañaveras JC, Wang J, Schmidt E, Zhang Z, TeSlaa T, Patel H, Chen L, Britt EC, Piqueras-Nebot M, Gomez-Cabrera MC, Lahoz A, Fan J, Beier UH, Kim H, Rabinowitz JD. A small molecule G6PD inhibitor reveals immune dependence on pentose phosphate pathway. Nat Chem Biol. 2020;16(7):731-9. doi: 10.1038/s41589-020-0533-x. PubMed PMID: 32393898; PMCID: PMC7311271.

Yang L, Garcia Canaveras JC, Chen Z, Wang L, Liang L, Jang C, Mayr JA, Zhang Z, Ghergurovich JM, Zhan L, Joshi S, Hu Z, McReynolds MR, Su X, White E, Morscher RJ, Rabinowitz JD. Serine Catabolism Feeds NADH when Respiration Is Impaired. Cell Metab. 2020;31(4):809-21.e6. doi: 10.1016/j.cmet.2020.02.017. PubMed PMID: 32187526; PMCID: PMC7397714.

Zhao S, Jang C, Liu J, Uehara K, Gilbert M, Izzo L, Zeng X, Trefely S, Fernandez S, Carrer A, Miller KD, Schug ZT, Snyder NW, Gade TP, Titchenell PM, Rabinowitz JD, Wellen KE. Dietary fructose feeds hepatic lipogenesis via microbiota-derived acetate. Nature. 2020;579(7800):586-91. doi: 10.1038/s41586-020-2101-7. PubMed PMID: 32214246; PMCID: PMC7416516.

Ghergurovich JM, Esposito M, Chen Z, Wang JZ, Bhatt V, Lan T, White E, Kang Y, Guo JY, Rabinowitz JD. Glucose-6-Phosphate Dehydrogenase Is Not Essential for K-Ras-Driven Tumor Growth or Metastasis. Cancer Res. 2020;80(18):3820-9. doi: 10.1158/0008-5472.Can-19-2486. PubMed PMID: 32661137; PMCID: PMC7501231.

Hui S, Cowan AJ, Zeng X, Yang L, TeSlaa T, Li X, Bartman C, Zhang Z, Jang C, Wang L, Lu W, Rojas J, Baur J, Rabinowitz JD. Quantitative Fluxomics of Circulating Metabolites. Cell Metab. 2020;32(4):676-88.e4. doi: 10.1016/j.cmet.2020.07.013. PubMed PMID: 32791100; PMCID: PMC7544659.

García-Cañaveras JC, Lancho O, Ducker GS, Ghergurovich JM, Xu X, da Silva-Diz V, Minuzzo S, Indraccolo S, Kim H, Herranz D, Rabinowitz JD. SHMT inhibition is effective and synergizes with methotrexate in T-cell acute lymphoblastic leukemia. Leukemia. 2021;35(2):377-88. doi: 10.1038/s41375-020-0845-6. PubMed PMID: 32382081; PMCID: PMC7647950.

Luongo TS, Eller JM, Lu MJ, Niere M, Raith F, Perry C, Bornstein MR, Oliphint P, Wang L, McReynolds MR, Migaud ME, Rabinowitz JD, Johnson FB, Johnsson K, Ziegler M, Cambronne XA, Baur JA. SLC25A51 is a mammalian mitochondrial NAD(+) transporter. Nature. 2020;588(7836):174-9. doi: 10.1038/s41586-020-2741-7. PubMed PMID: 32906142; PMCID: PMC7718333.

Martin JK, 2nd, Sheehan JP, Bratton BP, Moore GM, Mateus A, Li SH, Kim H, Rabinowitz JD, Typas A, Savitski MM, Wilson MZ, Gitai Z. A Dual-Mechanism Antibiotic Kills Gram-Negative Bacteria and Avoids Drug Resistance. Cell. 2020;181(7):1518-32.e14. doi: 10.1016/j.cell.2020.05.005. PubMed PMID: 32497502; PMCID: PMC7780349.

Zhang Y, Xu Y, Lu W, Ghergurovich JM, Guo L, Blair IA, Rabinowitz JD, Yang X. Upregulation of Antioxidant Capacity and Nucleotide Precursor Availability Suffices for Oncogenic Transformation. Cell Metab. 2021;33(1):94-109.e8. doi: 10.1016/j.cmet.2020.10.002. PubMed PMID: 33159852; PMCID: PMC7846267.

Guan D, Xiong Y, Trinh TM, Xiao Y, Hu W, Jiang C, Dierickx P, Jang C, Rabinowitz JD, Lazar MA. The hepatocyte clock and feeding control chronophysiology of multiple liver cell types. Science. 2020;369(6509):1388-94. doi: 10.1126/science.aba8984. PubMed PMID: 32732282; PMCID: PMC7849028.

Murashige D, Jang C, Neinast M, Edwards JJ, Cowan A, Hyman MC, Rabinowitz JD, Frankel DS, Arany Z. Comprehensive quantification of fuel use by the failing and nonfailing human heart. Science. 2020;370(6514):364-8. doi: 10.1126/science.abc8861. PubMed PMID: 33060364; PMCID: PMC7871704.

Chen L, Luo S, Dupre A, Vasoya RP, Parthasarathy A, Aita R, Malhotra R, Hur J, Toke NH, Chiles E, Yang M, Cao W, Flores J, Ellison CE, Gao N, Sahota A, Su X, Bonder EM, Verzi MP. The nuclear receptor HNF4 drives a brush border gene program conserved across murine intestine, kidney, and embryonic yolk sac. Nat Commun. 2021;12(1):2886. doi: 10.1038/s41467-021-22761-5. PubMed PMID: 34001900; PMCID: PMC8129143.

Cho S, Lee G, Pickering BF, Jang C, Park JH, He L, Mathur L, Kim SS, Jung S, Tang HW, Monette S, Rabinowitz JD, Perrimon N, Jaffrey SR, Blenis J. mTORC1 promotes cell growth via m(6)A-dependent mRNA degradation. Mol Cell. 2021;81(10):2064-75.e8. doi: 10.1016/j.molcel.2021.03.010. PubMed PMID: 33756105; PMCID: PMC8356906.

Ding H, Chen Z, Wu K, Huang SM, Wu WL, LeBoeuf SE, Pillai RG, Rabinowitz JD, Papagiannakopoulos T. Activation of the NRF2 antioxidant program sensitizes tumors to G6PD inhibition. Sci Adv. 2021;7(47):eabk1023. doi: 10.1126/sciadv.abk1023. PubMed PMID: 34788087; PMCID: PMC8598006.

Li SH, Nofal M, Parsons LR, Rabinowitz JD, Gitai Z. Monitoring mammalian mitochondrial translation with MitoRiboSeq. Nat Protoc. 2021;16(6):2802-25. doi: 10.1038/s41596-021-00517-1. PubMed PMID: 33953394; PMCID: PMC8610098.

Wilke AC, Doebele C, Zindel A, Lee KS, Rieke SA, Ceribelli M, Comoglio F, Phelan JD, Wang JQ, Pikman Y, Jahn D, Häupl B, Schneider C, Scheich S, Tosto FA, Bohnenberger H, Stauder P, Schnütgen F, Slabicki M, Coulibaly ZA, Wolf S, Bojarczuk K, Chapuy B, Brandts CH, Stroebel P, Lewis CA, Engelke M, Xu X, Kim H, Dang TH, et al. SHMT2 inhibition disrupts the TCF3 transcriptional survival program in Burkitt lymphoma. Blood. 2022;139(4):538-53. doi: 10.1182/blood.2021012081. PubMed PMID: 34624079; PMCID: PMC8938936.

Nofal M, Wang T, Yang L, Jankowski CSR, Hsin-Jung Li S, Han S, Parsons L, Frese AN, Gitai Z, Anthony TG, Wühr M, Sabatini DM, Rabinowitz JD. GCN2 adapts protein synthesis to scavenging-dependent growth. Cell Syst. 2022;13(2):158-72.e9. doi: 10.1016/j.cels.2021.09.014. PubMed PMID: 34706266; PMCID: PMC8961722.

Bartman CR, TeSlaa T, Rabinowitz JD. Quantitative flux analysis in mammals. Nat Metab. 2021;3(7):896-908. doi: 10.1038/s42255-021-00419-2. PubMed PMID: 34211182; PMCID: PMC9289955.

Zhang Y, Xu Y, Lu W, Li J, Yu S, Brown EJ, Stanger BZ, Rabinowitz JD, Yang X. G6PD-mediated increase in de novo NADP(+) biosynthesis promotes antioxidant defense and tumor metastasis. Sci Adv. 2022;8(29):eabo0404. doi: 10.1126/sciadv.abo0404. PubMed PMID: 35857842; PMCID: PMC9299539.

Xu Y, Zhang Y, García-Cañaveras JC, Guo L, Kan M, Yu S, Blair IA, Rabinowitz JD, Yang X. Chaperone-mediated autophagy regulates the pluripotency of embryonic stem cells. Science. 2020;369(6502):397-403. doi: 10.1126/science.abb4467. PubMed PMID: 32703873; PMCID: PMC7939502.

Ringel AE, Drijvers JM, Baker GJ, Catozzi A, García-Cañaveras JC, Gassaway BM, Miller BC, Juneja VR, Nguyen TH, Joshi S, Yao CH, Yoon H, Sage PT, LaFleur MW, Trombley JD, Jacobson CA, Maliga Z, Gygi SP, Sorger PK, Rabinowitz JD, Sharpe AH, Haigis MC. Obesity Shapes Metabolism in the Tumor Microenvironment to Suppress Anti-Tumor Immunity. Cell. 2020;183(7):1848-66.e26. doi: 10.1016/j.cell.2020.11.009. PubMed PMID: 33301708; PMCID: PMC8064125.

Park JO, Tanner LB, Wei MH, Khana DB, Jacobson TB, Zhang Z, Rubin SA, Li SH, Higgins MB, Stevenson DM, Amador-Noguez D, Rabinowitz JD. Near-equilibrium glycolysis supports metabolic homeostasis and energy yield. Nat Chem Biol. 2019;15(10):1001-8. doi: 10.1038/s41589-019-0364-9. PubMed PMID: 31548693.

Song Y, Park JO, Tanner L, Nagano Y, Rabinowitz JD, Shvartsman SY. Energy budget of Drosophila embryogenesis. Curr Biol. 2019;29(12):R566-r7. doi: 10.1016/j.cub.2019.05.025. PubMed PMID: 31211973; PMCID: PMC9665180.

Jankowski CSR, Rabinowitz JD. Selenium Modulates Cancer Cell Response to Pharmacologic Ascorbate. Cancer Res. 2022;82(19):3486-98. doi: 10.1158/0008-5472.Can-22-0408. PubMed PMID: 35916672; PMCID: PMC9532358.