Publications

2019

Notarangelo G, Haigis MC. Sweet Temptation: From Sugar Metabolism to Gene Regulation. Immunity. 2019 Dec 17;51(6):980-981. doi: 10.1016/j.immuni.2019.11.008.

Cable J, Finley L, Tu BP, Patti GJ, Oliver TG, Vardhana S, Mana M, Ericksen R, Khare S, DeBerardinis R, Stockwell BR, Edinger A, Haigis M, Kaelin W. Leveraging insights into cancer metabolism-a symposium report. Ann N Y Acad Sci. 2019 Dec 2. doi: 10.1111/nyas.14274.

Randall EC, Lopez BGC, Peng S, Regan MS, Abdelmoula WM, Basu SS, Santagata S, Yoon H, Haigis M, Agar JN, Tran NL, Elmquist WF, White FM, Sarkaria JN, Agar NYR. Localized metabolomic gradients in patient-derived xenograft models of glioblastoma. Cancer Res. 2019 Nov 25. pii: canres.0638.2019. doi: 10.1158/0008-5472.CAN-19-0638.

Ron-Harel N, Ghergurovich JM, Notarangelo G, LaFleur MW, Tsubosaka Y, Sharpe AH, Rabinowitz JD, Haigis MC. T Cell Activation Depends on Extracellular Alanine. Cell Rep. 2019 Sept 17;28(12):3011-3021.e4. doi: 10.1016/j.celrep.2019.08.034.

Wang H, Sheehan RP, Palmer AC, Everley RA, Boswell SA, Ron-Harel N, Ringel AE, Holton KM, Jacobson CA, Erickson AR, Maliszewski L, Haigis MC, Sorger PK. Adaptation of Human iPSC-Derived Cardiomyocytes to Tyrosine Kinase Inhibitors Reduces Acute Cardiotoxicity via Metabolic Reprogramming. Cell Syst. 2019 May 22;8(5):412-426.e7. doi: 10.1016/j.cels.2019.03.009. Epub 2019 May 8.

Chakraborty AA, Laukka T, Myllykoski M, Ringel AE, Booker MA, Tolstorukov MY, Meng YJ, Meier SR, Jennings RB, Creech AL, Herbert ZT, McBrayer SK, Olenchock BA, Jaffe JD, Haigis MC, Beroukhim R, Signoretti S, Koivunen P, Kaelin WG Jr. Histone demethylase KDM6A directly senses oxygen to control chromatin and cell fate. Science. 2019 Mar 15;363(6432):1217-1222. doi: 10.1126/science.aaw1026. Epub 2019 Mar 14.

2018

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. 26;115(52):13347-13352. doi: 10.1073/pnas.1804149115. PMID:30530686.

Ringel AE, Tucker SA, Haigis MC. Chemical and Physiological Features of Mitochondrial Acylation. Mol Cell. 2018. 15;72(4):610-624. doi: 10.1016/j.molcel.2018.10.023. PMID: 30444998.

McBrayer SK, Mayers JR, DiNatale GJ, Shi DD, Khanal J, Chakraborty AA, Sarosiek KA, Briggs KJ, Robbins AK, Sewastianik T, Shareef SJ, Olenchock BA, Parker SJ, Tateishi K, Spinelli JB, Islam M, Haigis MC, Looper RE, Ligon KL, Bernstein BE, Carrasco RD, Cahill DP, Asara JM, Metallo CM, Yennawar NH, Vander Heiden MG, Kaelin WG Jr. Transaminase Inhibition by 2-Hydroxyglutarate Impairs Glutamate Biosynthesis and Redox Homeostasis in Glioma. Cell. 2018. 175(1):101-116.e25. doi: 10.1016/j.cell.2018.08.038. PMID:30220459

Adachi Y, De Sousa-Coelho AL, Harata I, Aoun C, Weimer S, Shi X, Gonzalez Herrera KN, Takahashi H, Doherty C, Noguchi Y, Goodyear LJ, Haigis MC, Gerszten RE, Patti ME. l-Alanine activates hepatic AMP-activated protein kinase and modulates systemic glucose metabolism. Mol Metab. 2018. 17:61-70. doi: 10.1016/j.molmet.2018.08.002. PMID:30190193

Lee JJ, van de Ven RAH, Zaganjor E, Ng MR, Barakat A, Demmers JJPG, Finley LWS, Gonzalez Herrera KN, Hung YP, Harris IS, Jeong SM, Danuser G, McAllister SS, Haigis MC. Inhibition of epithelial cell migration and Src/FAK signaling by SIRT3. Proc Natl Acad Sci U S A. 2018;115(27):7057-7062. doi: 10.1073/pnas.1800440115. PMID:2991502

Mills EL, Pierce KA, Jedrychowski MP, Garrity R, Winther S, Vidoni S, Yoneshiro T, Spinelli JB, Lu GZ, Kazak L, Banks AS, Haigis MC, Kajimura S, Murphy MP, Gygi SP, Clish CB, Chouchani ET. Accumulation of succinate controls activation of adipose tissue thermogenesis. Nature. 2018. doi: 10.1038/s41586-018-0353-2. PMID:30022159

Spinelli JB, Haigis MC. The multifaceted contributions of mitochondria to cellular metabolism. Nat Cell Biol. 2018, 20(7):745-754. doi: 10.1038/s41556-018-0124-1. PMID: 29950572

Escudero S, Zaganjor E, Lee S, Mill CP, Morgan AM, Crawford EB, Chen J, Wales TE, Mourtada R, Luccarelli J, Bird GH, Steidl U, Engen JR, Haigis MC, Opferman JT6, Walensky LD. Dynamic Regulation of Long-Chain Fatty Acid Oxidation by a Noncanonical Interaction between the MCL-1 BH3 Helix and VLCAD. Mol Cell. 2018;69:729-743. PMID: 29499131

Gonzalez Herrera KN, Zaganjor E, Ishikawa Y, Spinelli JB, Yoon H, Lin JR, Satterstrom FK, Ringel A, Mulei S, Souza A, Gorham JM, Benson CC, Seidman JG, Sorger PK, Clish CB, Haigis MC. Small-Molecule Screen Identifies De Novo Nucleotide Synthesis as a Vulnerability of Cells Lacking SIRT3. Cell Rep. 2018;22:1945-1955. PMID: 29466723

2017

Spinelli JB, Yoon H, Ringel AE, Jeanfavre S, Clish CB, Haigis MC. Metabolic recycling of ammonia via glutamate dehydrogenase supports breast cancer biomass. Science. 2017;358:941-946. PMID: 29025995

Malone CF, Emerson C, Ingraham R, Barbosa W, Guerra S, Yoon H, Liu LL, Michor F, Haigis MC, Macleod KF, Maertens O, Cichowski K. mTOR and HDAC Inhibitors Converge on the TXNIP/Thioredoxin Pathway to Cause Catastrophic Oxidative Stress and Regression of RAS-Driven Tumors. Cancer Discov. 2017;7:1450-1463. PMID: 28963352

Spinelli JB, Kelley LP, Haigis MC. An LC-MS Approach to Quantitative Measurement of Ammonia Isotopologues. Sci Rep. 2017;7:10304. PMID: 28871132

Zaganjor E, Spinelli JB, Haigis MC. Strength in numbers: Phosphofructokinase polymerization prevails in the liver. J Cell Biol. 2017;216:2239-2241. PMID: 28716843

Zaganjor E, Vyas S, Haigis MC. SIRT4 Is a Regulator of Insulin Secretion. Cell Chem Biol. 2017;24:656-658. PMID: 28644956

van de Ven RA, Santos D, Haigis MC. Mitochondrial Sirtuins and Molecular Mechanisms of Aging. Trends Mol Med. 2017;17:30024-2. Review. PMID: 28285806

2016

Yang W, Nagasawa K, Münch C, Xu Y, Satterstrom K, Jeong S, Hayes SD, Jedrychowski MP, Vyas FS, Zaganjor E, Guarani V, Ringel AE, Gygi SP, Harper JW, Haigis MC. Mitochondrial Sirtuin Network Reveals Dynamic SIRT3-Dependent Deacetylation in Response to Membrane Depolarization. Cell. 2016;167, 985–1000. PMID: 27881304

Sage PT, Ron-Harel N, Juneja VR, Sen DR, Maleri S, Sungnak W, Kuchroo VK, Haining WN, Chevrier N, Haigis MC, Sharpe AH. Suppression by TFR cells leads to durable and selective inhibition of B cell effector function. Nat Immunol. 2016;12:1436-1446. PMID: 27695002

German NJ, Yoon H, Yusuf RZ, Murphy JP, Finley LW, Laurent G, Haas W, Satterstrom FK, Guarnerio J, Zaganjor E, Santos D, Pandolfi PP, Beck AH, Gygi SP, Scadden DT, Kaelin WG Jr, Haigis MC. PHD3 Loss in Cancer Enables Metabolic Reliance on Fatty Acid Oxidation via Deactivation of ACC2. Mol Cell. 2016;63:1006-1020. PMID: 27635760

Vyas S, Zaganjor  E, Haigis MC. Mitochondria and Cancer. Cell. 2016;166:555-566. Review. PMID: 27471965 (http://www.sciencedirect.com/science/article/pii/S0092867416309084)

Mitochondria and Cancer, Cell, Review

Ron-Harel N, Santos D, Ghergurovich JM, Sage PT, Reddy A, Lovitch SB, Dephoure N, Satterstrom FK, Sheffer M, Spinelli JB, Gygi S, Rabinowitz JD, Sharpe AH, Haigis MC. Mitochondrial Biogenesis and Proteome Remodeling Promote One-Carbon Metabolism for T Cell Activation. Cell Metab. 2016;24:104-417. PMID: 27411012

2015

Jeong SM, Haigis MC. Sirtuins in Cancer: a Balancing Act between Genome Stability and Metabolism. Mol Cells. 2015;38:750-758. Review. PMID: 26420294

Sage PT, Tan CL, Freeman GJ, Haigis M, Sharpe AH. Defective TFH Cell Function and Increased TFR Cells Contribute to Defective Antibody Production in Aging. Cell Rep. 2015;12:163-171. PMID: 26146074

German NJ, Haigis MC. Sirtuins and the Metabolic Hurdles in Cancer. Curr Biol. 2015;25:R569-583. Review. PMID: 26126285

Satterstrom FK, Swindell WR, Laurent G, Vyas S, Bulyk ML, Haigis MC. Nuclear respiratory factor 2 induces SIRT3 expression. Aging Cell. 2015;14:818-825. PMID: 26109058

Gonzalez Herrera KN, Lee J, Haigis MC. Intersections between mitochondrial sirtuin signaling and tumor cell metabolism. Crit Rev Biochem Mol Biol. 2015;50:242-255. PMID: 25898275

Ron-Harel N, Sharpe AH, Haigis MC. Mitochondrial metabolism in T cell activation and senescence: a mini-review. Gerontology. 2015;61:131-138. PMID: 25402204

2014

LeBleu VS, O'Connell JT, Gonzalez Herrera KN, Wikman H, Pantel K, Haigis MC, de Carvalho FM, Damascena A, Domingos Chinen LT, Rocha RM, Asara JM, Kalluri R. PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat Cell Biol. 2014;16:992-1003. PMID: 25241037

Janzer A, German NJ, Gonzalez-Herrera KN, Asara JM, Haigis MC, Struhl K. Metformin and phenformin deplete tricarboxylic acid cycle and glycolytic intermediates during cell transformation and NTPs in cancer stem cells. Proc Natl Acad Sci U S A. 2014; 111:10574-10579. PMID: 25002509

Sinkevicius KW, Kriegel C, Bellaria KJ, Lee J, Lau AN, Leeman KT, Zhou P, Beede AM, Fillmore CM, Caswell D, Barrios J, Wong KK, Sholl LM, Schlaeger TM, Bronson RT, Chirieac LR, Winslow MM, Haigis MC, Kim CF. Neurotrophin receptor TrkB promotes lung adenocarcinoma metastasis. Proc Natl Acad Sci U S A. 2014; 111:10299-10304. PMID: 24982195

Satterstrom FK, Haigis MC. Luciferase-based reporter to monitor the transcriptional activity of the SIRT3 promoter. Methods Enzymol. 2014; 543:141-163. PMID: 24924131

Jeong SM, Lee J, Finley LW, Schmidt PJ, Fleming MD, Haigis MC. SIRT3 regulates cellular iron metabolism and cancer growth by repressing iron regulatory protein 1. Oncogene. 2014 Jun 9. [Epub ahead of print] PMID: 24909164

Jeong SM, Lee A, Lee J, Haigis MC. SIRT4 protein suppresses tumor formation in genetic models of Myc-induced B cell lymphoma. J Biol Chem. 2014; 289:4135-4144. PMID: 24368766

2013

Bause AS, Matsui MS, Haigis MC. The Protein Deacetylase SIRT3 Prevents Oxidative Stress-induced Keratinocyte Differentiation. J Biol Chem. 2013; 288:36484-36491. PMID: 24194516

Laurent G, de Boer VC, Finley LW, Sweeney M, Lu H, Schug TT, Cen Y, Jeong SM, Li X, Sauve AA, Haigis MC. SIRT4 represses peroxisome proliferator-activated receptor α activity to suppress hepatic fat oxidation. Mol Cell Biol. 2013; 33:4552-4561. PMID: 24043310

Yang MH, Laurent G, Bause AS, Spang R, German N, Haigis MC, Haigis KM. HDAC6 and SIRT2 regulate the acetylation state and oncogenic activity of mutant K-RAS. Mol Cancer Res. 2013; 11:1072-1077. PMID: 23723075

Laurent G., German NJ, Saha AK, de Boer VCJ, Davies M, Koves TR, Dephoure N, Fischer F, Boanca G, Vaitheesvaran B, Lovitch SB, Sharpe AH, Kurland IJ, Steegborn C, Gygi SP, Muoio DM, Ruderman NB, Haigis MC. SIRT4 coordinates the balance between lipid synthesis and catabolism by repressing malonyl-CoA decarboxylase. Molecular Cell. 2013; 50:686-698. PMID: 23746352

Csibi A, Fendt SM, Li C, Poulogiannis G, Choo AY, Chapski DJ, Jeong SM, Dempsey JM, Parkhitko A, Morrison T, Henske EP, Haigis MC, Cantley LC, Stephanopoulos G, Yu J, Blenis J. The mTORC1 Pathway Stimulates Glutamine Metabolism and Cell Proliferation by Repressing SIRT4. Cell. 2013; 153:840-854. PMID: 23663782

Jeong SM, Xiao C, Finley LW, Lahusen T, Souza AL, Pierce K, Li YH, Wang X, Laurent G, German NJ, Xu X, Li C, Wang RH, Lee J, Csibi A, Cerione R, Blenis J, Clish CB, Kimmelman A, Deng CX, Haigis MC. SIRT4 Has Tumor-Suppressive Activity and Regulates the Cellular Metabolic Response to DNA Damage by Inhibiting Mitochondrial Glutamine Metabolism. Cancer Cell. 2013; 23:450-463. PMID: 23562301

Son J, Lyssiotis CA, Ying H, Wang X, Hua S, Ligorio M, Perera RM, Ferrone CR, Mullarky E, Shyh-Chang N, Kang Y, Fleming JB, Bardeesy N, Asara JM, Haigis MC, DePinho RA, Cantley LC, Kimmelman AC. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature. 2013; 496:101-105. PMID: 23535601

Lee PC, Dodart JC, Aron L, Finley LW, Bronson RT, Haigis MC, Yankner BA, Harper JW. Altered Social Behavior and Neuronal Development in Mice Lacking the Uba6-Use1 Ubiquitin Transfer System. Mol Cell. 2013; 50:172-184. PMID: 23499007

Peserico A, Chiacchiera F, Grossi V, Matrone A, Latorre D, Simonatto M, Fusella A, Ryall JG, Finley LW, Haigis MC, Villani G, Puri PL, Sartorelli V, Simone C. A novel AMPK-dependent FoxO3A-SIRT3 intramitochondrial complex sensing glucose levels. Cell Mol Life Sci. 2013; 70:2015-2029. PMID: 23283301

2012

Sebastian C, Satterstrom KF, Haigis MC, Mostoslavsky R. From Sirtuin biology to human diseases: an update. J Biol Chem. 2012; 287:42444-42452. Review. PMID: 23086954

Bause AS, Haigis MC. SIRT3 regulation of mitochondrial oxidative stress. Exp Gerontol. 2012; [Epub ahead of print] PMID: 22964489

Carracedo A, Weiss D, Leliaert AK, Bhasin M, de Boer VC, Laurent G, Adams AC, Sundvall M, Song SJ, Ito K, Finley LS, Egia A, Libermann T, Gerhart-Hines Z, Puigserver P, Haigis MC, Maratos-Flier E, Richardson AL, Schafer ZT, Pandolfi PP. A metabolic prosurvival role for PML in breast cancer. J Clin Invest. 2012; 122:3088-3100. PMID: 22886304

Inuzuka H, Gao D, Finley LW, Yang W, Wan L, Fukushima H, Chin YR, Zhai B, Shaik S, Lau AW, Wang Z, Gygi SP, Nakayama K, Teruya-Feldstein J, Toker A, Haigis MC, Pandolfi PP, Wei W. Acetylation-dependent regulation of Skp2 function. Cell. 2012; 150:179-193. PMID: 22770219

Finley LW, Haigis MC. Metabolic regulation by SIRT3: implications for tumorigenesis. Trends Mol Med. 2012; 18:516-523. PMID: 22749020

Yang MH, Nickerson S, Kim ET, Liot C, Laurent G, Spang R, Philips MR, Shan Y, Shaw DE, Bar-Sagi D, Haigis MC, Haigis KM. Regulation of RAS oncogenicity by acetylation. Proc Natl Acad Sci U S A. 2012; 109:10843-10848. PMID: 22711838

Haigis MC, Deng CX, Finley LW, Kim HS, Gius D. SIRT3 is a mitochondrial tumor suppressor: a scientific tale that connects aberrant cellular ROS, the Warburg effect, and carcinogenesis. Cancer Res. 2012; 72:2468-2472. PMID: 22589271

Cerletti M, Jang YC, Finley LW, Haigis MC, Wagers AJ. Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell. 2012; 10:515-519. PMID: 22560075

Garcia-Cao I, Song MS, Hobbs RM, Laurent G, Giorgi C, de Boer VC, Anastasiou D, Ito K, Sasaki AT, Rameh L, Carracedo A, Vander Heiden MG, Cantley LC, Pinton P, Haigis MC, Pandolfi PP. Systemic elevation of PTEN induces a tumor-suppressive metabolic state. Cell. 2012; 149:49-62. PMID: 22401813

Finley LW, Lee J, Souza A, Desquiret-Dumas V, Bullock K, Rowe GC, Procaccio V, Clish CB, Arany Z, Haigis MC. Skeletal muscle PGC-1alpha mediates mitochondrial, but not metabolic, adaptation to calorie restriction. Proc Natl Acad Sci U S A. 2012; 109:2931-2936. PMID: 22308395

2011

De Raedt T, Walton Z, Lucas J, Li D, Chen Y, Maertens O, Jeong SM, Bronson RT, Normant E, Haigis MC, Manning BD, Wong KK, Macleod KF, and Cichowski K. Developing an mTOR-inhibitor based combination cancer therapy. Cancer Cell. 2011; 20:400-413. PMID 21907929.

Finley LW, Haas W, Desquiret-Dumas V, Wallace DC, Procaccio V, Gygi SP, Haigis MC. Succinate dehydrogenase is a direct target of sirtuin 3 deacetylase activity. PLoS One. 2011; 6:e23295. PMID: 21858060.

Yang S, Wang X, Contino G, Liesa M, Sahin E, Ying H, Bause A, Li Y, Stommel JM, Deill’antonio G, Mautner J, Tonon G, Haigis M, Shirihai OS, Doglioni C, Bardeesy N, Kimmelman AC. Pancreatic cancers require autophagy for growth. Genes Dev. 2011; 25:717-729. PMID 21406549.

Finley LW, Carracedo A, Lee J, Souza A, Egia A, Zhang J, Teruya-Feldstein J, Moreira PI, Cardosa SM, Clish CB, Pandolfi PP, Haigis MC. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell. 2011; 19:416-428. PMID: 21397863.

2010

Haigis MC, Yankner BA. The aging stress response. Mol. Cell. 2010; 40:333-344. PMID: 20965426.

Haigis MC, Sinclair DA. Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol. 2010; 5:253-295. PMID: 20078221.

2009

Finley LS and Haigis MC. The coordination of nuclear and mitochondrial communication during aging and calorie restriction. Aging Research Reviews. 2009; 8:173-188.

Nakagawa T, Lomb D, Haigis MC, Guarente. SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell. 2009; 3:560-570.

2008

Haigis KM, Kendall KR, Wang Y, Cheung A, Haigis MC, Glickman JN, Niwa-Kawakita M, Sweet-Cordero A, Sebolt-Leopold J, Shannon KM, Settleman J, Giovannini M, Jacks T. Differential effects of oncogenic K-Ras and N-Ras on proliferation, differentiation, and tumor progression in the colon. Nature Genetics. 2008; 40:600-608.

2007

Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, Kim J, Yancopoulos G, Valenzuela D, Murphy A, Yang Y, Chen Y, Hirschey MD, Bronson RT, Haigis M, Guarente LP, Farese RV Jr, Weissman S, Verdin E, Schwer B. Mammalian Sir2 Homolog SIRT3 Regulates Global lysine acetylation. Mol Cell Biol. 2007; 27:8807-8814.

2006

Haigis MC, Guarente L. Mammalian sirtuins-emerging roles in physiology, aging and calorie restriction. Genes and Development. 2006; 20:2913-2921.

Haigis MC, Mostoslavsky R, Haigis KM, Fahie K, Christodoulou DC, Murphy AJ, Valenzuela DM, Yancopoulos GD, Karow M, Blander G, Wolberger C, Prolla TA, Weindruch R, Alt FW, Guarente L. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell. 2006; 126:941-954.

2005

Blander G, Olejnik, Krzymanska-Olejnik, McDonagh T, Haigis MC, Yaffe M, Guarente L. SIRT1 shows no substrate specificity in vitro. Journal of Biological Chemistry. 2005; 280:9780-9785.

2004

Leissring M, Farris W, Wu, Christodoulou D, Haigis MC, Guarente L, Selkoe D. Alternative translation initiation generates a novel isoform of insulin-degrading enzyme targeted to mitochondria. Biochemical Journal. 2004; 116:313-324.

Lin SJ, Ford E, Haigis MC, Liszt G, Guarente L. Calorie restriction extends yeast life span by lowering the level of NADH. Genes and Development. 2004; 18:12-16.

2003

Blander G, de Oliveira R, Conboy C, Haigis MC, Guarente L. Superoxide dismutase I knock-down induces senescence in human fibroblasts. Journal of Biological Chemistry. 2003; 278:38966-38969.