Akt-mTORC1 signaling regulates Acly to integrate metabolic input to control of macrophage activation

eLife

Volumn 5, Issue FEBRUARY2016, 2016, Pages

  Covarrubias, Anthony J ^a   Aksoylar, Halil Ibrahim ^a   Yu, Jiujiu ^a   Snyder, Nathaniel W ^b,c   Worth, Andrew J ^b   Iyer, Shankar S ^d   Wang, Jiawei ^e   Ben Sahra, Issam ^a   Byles, Vanessa ^a   Polynne Stapornkul, Tiffany ^a   Espinosa, Erika C ^a   Lamming, Dudley ^f   Manning, Brendan D ^a   Zhang, Yijing ^e   Blair, Ian A ^b   Horng, Tiffany ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DREXEL UNIVERSITY   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^f UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 4; JANUS KINASE 1; JANUS KINASE 3; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN KINASE; PROTEIN KINASE B; STAT6 PROTEIN; ADENOSINE TRIPHOSPHATE CITRATE SYNTHASE; CHEMOKINE; HISTONE; IL4 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FATTY ACID OXIDATION; GENE EXPRESSION; GENE LIBRARY; GENE MAPPING; GENETIC ANALYSIS; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; LIQUID CHROMATOGRAPHY; LUCIFERASE ASSAY; MACROPHAGE ACTIVATION; MASS SPECTROMETRY; METABOLOMICS; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ACETYLATION; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; MACROPHAGE; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING;

ACETYLATION; ANIMALS; ATP CITRATE (PRO-S)-LYASE; CELL PROLIFERATION; CHEMOKINES; GENE EXPRESSION REGULATION; HISTONES; INTERLEUKIN-4; MACROPHAGE ACTIVATION; MACROPHAGES; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MICE, INBRED C57BL; MULTIPROTEIN COMPLEXES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84961281785     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.11612     Document Type: Article

References (52)

1. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11:R106. doi: 10.1186/gb-2010-11-10-r106
2. Basu SS, Blair IA. 2012. SILEC: a protocol for generating and using isotopically labeled coenzyme a mass spectrometry standards. Nature Protocols 7:1-12. doi: 10.1038/nprot.2011.421
3. Basu SS, Mesaros C, Gelhaus SL, Blair IA. 2011. Stable isotope labeling by essential nutrients in cell culture for preparation of labeled coenzyme a and its thioesters. Analytical Chemistry 83:1363-1369. doi: 10.1021/ac1027353
4. Ben-Sahra I, Howell JJ, Asara JM, Manning BD. 2013. Stimulation of de novo pyrimidine synthesis by growth signaling through mTOR and S6K1. Science 339:1323-1328. doi: 10.1126/science.1228792
5. Berwick DC, Hers I, Heesom KJ, Moule SK, Tavare JM. 2002. The identification of ATP-citrate lyase as a protein kinase b (akt) substrate in primary adipocytes. Journal of Biological Chemistry 277:33895-33900. doi: 10.1074/jbc.M204681200
6. Biswas SK, Mantovani A. 2012. Orchestration of metabolism by macrophages. Cell Metabolism 15:432-437. doi: 10.1016/j.cmet.2011.11.013
7. Byles V, Covarrubias AJ, Ben-Sahra I, Lamming DW, Sabatini DM, Manning BD, Horng T. 2013. The TSC-mTOR pathway regulates macrophage polarization. Nature Communications 4:2834. doi: 10.1038/ncomms3834
8. Carey BW, Finley LWS, Cross JR, Allis CD, Thompson CB. 2015. Intracellular a-ketoglutarate maintains the pluripotency of embryonic stem cells. Nature 518:413-416. doi: 10.1038/nature13981
9. Cheng SC, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, Giamarellos-Bourboulis EJ, Martens JH, Rao NA, Aghajanirefah A, Manjeri GR, Li Y, Ifrim DC, Arts RJ, van der Veer BM, van der Meer BM, Deen PM, Logie C, O’Neill LA, Willems P, van de Veerdonk FL, van der Meer JW, Ng A, Joosten LA, Wijmenga C, Stunnenberg HG, Xavier RJ, Netea MG. 2014. MTOR- and HIF-1a-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345:1250684. doi: 10.1126/science.1250684
10. Cormier SA, Yuan S, Crosby JR, Protheroe CA, Dimina DM, Hines EM, Lee NA, Lee JJ. 2002. Th2-mediated pulmonary inflammation leads to the differential expression of ribonuclease genes by alveolar macrophages. American Journal of Respiratory Cell and Molecular Biology 27:678-687. doi: 10.1165/rcmb.4882
11. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber H-P, Ferrara N, Johnson RS. 2003. HIF-1 is essential for myeloid cell-mediated inflammationn. Cell 112:645-657. doi: 10.1016/S0092-8674(03)00154-5
12. Davies LC, Jenkins SJ, Allen JE, Taylor PR. 2013. Tissue-resident macrophages. Nature Immunology 14:986-995. doi: 10.1038/ni.2705
13. Dibble CC, Manning BD. 2013. Signal integration by mTORC1 coordinates nutrient input with biosynthetic output. Nature Cell Biology 15:555-564. doi: 10.1038/ncb2763
14. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, Triantafellow E, Ma Q, Gorski R, Cleaver S, Vander Heiden MG, MacKeigan JP, Finan PM, Clish CB, Murphy LO, Manning BD. 2010. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Molecular Cell 39:171-183. doi: 10.1016/j.molcel.2010.06.022
15. Everts B, Amiel E, Huang SC-C, Smith AM, Chang C-H, Lam WY, Redmann V, Freitas TC, Blagih J, van der Windt GJW, Artyomov MN, Jones RG, Pearce EL, Pearce EJ. 2014. TLR-driven early glycolytic reprogramming via the kinases TBK1-IKK" supports the anabolic demands of dendritic cell activation. Nature Immunology 15:323-332. doi: 10.1038/ni.2833
16. Finlay D, Cantrell DA. 2011. Metabolism, migration and memory in cytotoxic t cells. Nature Reviews Immunology 11:109-117. doi: 10.1038/nri2888
17. Galván-Peña S, O’Neill LA.2014.Metabolic reprogramming in macrophage polarization. Frontiersin Immunology 5:420. doi: 10.3389/fimmu.2014.00420
18. Gut P, Verdin E. 2013. The nexus of chromatin regulation and intermediary metabolism. Nature 502:489-498. doi: 10.1038/nature12752
19. Hallows WC, Lee S, Denu JM. 2006. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proceedings of the National Academy of Sciences of the United States of America 103:10230-10235. doi: 10.1073/pnas.0604392103
20. Hara K, Yonezawa K, Weng Q-P, Kozlowski MT, Belham C, Avruch J. 1998. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. Journal of Biological Chemistry 273:14484-14494. doi: 10.1074/jbc.273.23.14484
21. Hotamisligil GS, Erbay E. 2008. Nutrient sensing and inflammation in metabolic diseases. Nature Reviews Immunology 8:923-934. doi: 10.1038/nri2449
22. Huang DW, Sherman BT, Lempicki RA. 2008. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4:44-57. doi: 10.1038/nprot.2008.211
23. Jha AK, Huang SC-C, Sergushichev A, Lampropoulou V, Ivanova Y, Loginicheva E, Chmielewski K, Stewart KM, Ashall J, Everts B, Pearce EJ, Driggers EM, Artyomov MN. 2015. Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization. Immunity 42:419-430. doi: 10.1016/j.immuni.2015.02.005
24. Kaelin WG, McKnight SL. 2013. Influence of metabolism on epigenetics and disease. Cell 153:56-69. doi: 10.1016/j.cell.2013.03.004
25. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10:R25. doi: 10.1186/gb-2009-10-3-r25
26. Laplante M, Sabatini DM. 2012. MTOR signaling in growth control and disease. Cell 149:274-293. doi: 10.1016/j.cell.2012.03.017
27. Lee JV, Carrer A, Shah S, Snyder NW, Wei S, Venneti S, Worth AJ, Yuan Z-F, Lim H-W, Liu S, Jackson E, Aiello NM, Haas NB, Rebbeck TR, Judkins A, Won K-J, Chodosh LA, Garcia BA, Stanger BZ, Feldman MD, Blair IA, Wellen KE. 2014. Akt-dependent metabolic reprogramming regulates tumor cell histone acetylation. Cell Metabolism 20:306-319. doi: 10.1016/j.cmet.2014.06.004
28. Mariño G, Pietrocola F, Eisenberg T, Kong Y, Malik SA, Andryushkova A, Schroeder S, Pendl T, Harger A, Niso- Santano M, Zamzami N, Scoazec M, Durand S, Enot DP, Fernández Álvaro F., Martins I, Kepp O, Senovilla L, Bauvy C, Morselli E, Vacchelli E, Bennetzen M, Magnes C, Sinner F, Pieber T, López-Otín C, Maiuri MC, Codogno P, Andersen JS, Hill JA, Madeo F, Kroemer G. 2014. Regulation of autophagy by cytosolic acetyl-coenzyme a. Molecular Cell 53:710-725. doi: 10.1016/j.molcel.2014.01.016
29. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nature Methods 5:621-628. doi: 10.1038/nmeth.1226
30. Murray PJ, Wynn TA. 2011. Protective and pathogenic functions of macrophage subsets. Nature Reviews Immunology 11:723-737. doi: 10.1038/nri3073
31. Novellasdemunt L, Tato I, Navarro-Sabate A, Ruiz-Meana M, Mendez-Lucas A, Perales JC, Garcia-Dorado D, Ventura F, Bartrons R, Rosa JL. 2013. Akt-dependent activation of the heart 6-phosphofructo-2-kinase/Fructose-2,6-bisphosphatase (pFKFB2) isoenzyme by amino acids. Journal of Biological Chemistry 288:10640-10651. doi: 10.1074/jbc.M113.455998
32. Odegaard JI, Chawla A. 2011. Alternative macrophage activation and metabolism. Annual Review of Pathology: Mechanisms of Disease 6:275-297. doi: 10.1146/annurev-pathol-011110-130138
33. Pearce EJ, Everts B. 2015. Dendritic cell metabolism. Nature Reviews Immunology 15:18-29. doi: 10.1038/nri3771
34. Pietrocola F, Galluzzi L, Bravo-San Pedro JM, Madeo F, Kroemer G. 2015. Acetyl coenzyme a: a central metabolite and second messenger. Cell Metabolism 21:805-821. doi: 10.1016/j.cmet.2015.05.014
35. Pollizzi KN, Powell JD. 2014. Integrating canonical and metabolic signalling programmes in the regulation of t cell responses. Nature Reviews Immunology 14:435-446. doi: 10.1038/nri3701
36. Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S, Griffiths JR, Chung Y-L, Schulze A. 2008. SREBP activity is regulated by mTORC1 and contributes to akt-dependent cell growth. Cell Metabolism 8:224-236. doi: 10.1016/j.cmet.2008.07.007
37. Robey RB, Hay N. 2009. Is akt the "warburg kinase"?—akt-energy metabolism interactions and oncogenesis. Seminars in Cancer Biology 19:25-31. doi: 10.1016/j.semcancer.2008.11.010
38. Ruckerl D, Jenkins SJ, Laqtom NN, Gallagher IJ, Sutherland TE, Duncan S, Buck AH, Allen JE. 2012. Induction of IL-4R-dependent microRNAs identifies PI3K/Akt signaling as essential for IL-4-driven murine macrophage proliferation in vivo. Blood 120:2307-2316. doi: 10.1182/blood-2012-02-408252
39. Sengupta S, Peterson TR, Laplante M, Oh S, Sabatini DM. 2010. MTORC1 controls fasting-induced ketogenesis and its modulation by ageing. Nature 468:1100-1104. doi: 10.1038/nature09584
40. Shimazu T, Hirschey MD, Newman J, He W, Shirakawa K, Le Moan N, Grueter CA, Lim H, Saunders LR, Stevens RD, Newgard CB, Farese RV, de Cabo R, Ulrich S, Akassoglou K, Verdin E. 2013. Suppression of oxidative stress by-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 339:211-214. doi: 10.1126/science.1227166
41. Snyder NW, Tombline G, Worth AJ, Parry RC, Silvers JA, Gillespie KP, Basu SS, Millen J, Goldfarb DS, Blair IA. 2015. Production of stable isotope-labeled acyl-coenzyme a thioesters by yeast stable isotope labeling by essential nutrients in cell culture. Analytical Biochemistry 474:59-65. doi: 10.1016/j.ab.2014.12.014
42. Sutendra G, Kinnaird A, Dromparis P, Paulin R, Stenson TH, Haromy A, Hashimoto K, Zhang N, Flaim E, Michelakis ED. 2014. A nuclear pyruvate dehydrogenase complex is important for the generation of acetyl-CoA and histone acetylation. Cell 158:84-97. doi: 10.1016/j.cell.2014.04.046
43. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, Frezza C, Bernard NJ, Kelly B, Foley NH, Zheng L, Gardet A, Tong Z, Jany SS, Corr SC, Haneklaus M, Caffrey BE, Pierce K, Walmsley S, Beasley FC, Cummins E, Nizet V, Whyte M, Taylor CT, Lin H, Masters SL, Gottlieb E, Kelly VP, Clish C, Auron PE, Xavier RJ, O’Neill LAJ. 2013. Succinate is an inflammatory signal that induces IL-1 through HIF-1a. Nature 496:238-242. doi: 10.1038/nature11986
44. Tato I, Bartrons R, Ventura F, Rosa JL. 2011. Amino acids activate mammalian target of rapamycin complex 2 (mTORC2) via PI3K/Akt signaling. Journal of Biological Chemistry 286:6128-6142. doi: 10.1074/jbc.M110.166991
45. Teperino R, Schoonjans K, Auwerx J. 2010. Histone methyl transferases and demethylases; can they link metabolism and transcription? Cell Metabolism 12:321-327. doi: 10.1016/j.cmet.2010.09.004
46. Van Dyken SJ, Locksley RM. 2013. Interleukin-4- and interleukin-13-mediated alternatively activated macrophages: roles in homeostasis and disease. Annual Review of Immunology 31:317-343. doi: 10.1146/annurev-immunol-032712-095906
47. Vats D, Mukundan L, Odegaard JI, Zhang L, Smith KL, Morel CR, Wagner RA, Greaves DR, Murray PJ, Chawla A. 2006. Oxidative metabolism and PGC-1 attenuate macrophage-mediated inflammationn. Cell Metabolism 4: 13-24. doi: 10.1016/j.cmet.2006.05.011
48. Weichhart T, Costantino G, Poglitsch M, Rosner M, Zeyda M, Stuhlmeier KM, Kolbe T, Stulnig TM, Horl WH, Hengstschlager M, Muller M, Saemann MD. 2008. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 29:565-577. doi: 10.1016/j.immuni.2008.08.012
49. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB. 2009. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324:1076-1080. doi: 10.1126/science.1164097
50. Worth AJ, Basu SS, Snyder NW, Mesaros C, Blair IA. 2014. Inhibition of neuronal cell mitochondrial complex i with rotenone increases lipid-oxidation, supporting acetyl-coenzyme a levels. Journal of Biological Chemistry 289:26895-26903. doi: 10.1074/jbc.M114.591354
51. Yamada KJ, Barker T, Dyer KD, Rice TA, Percopo CM, Garcia-Crespo KE, Cho S, Lee JJ, Druey KM, Rosenberg HF. 2015. Eosinophil-associated ribonuclease 11 is a macrophage chemoattractant. Journal of Biological Chemistry 290:8863-8875. doi: 10.1074/jbc.M114.626648
52. Zhu L, Yang T, Li L, Sun L, Hou Y, Hu X, Zhang L, Tian H, Zhao Q, Peng J, Zhang H, Wang R, Yang Z, Zhang L, Zhao Y. 2014. TSC1 controls macrophage polarization to prevent inflammatory disease. Nature Communications 5:4696. doi: 10.1038/ncomms569.