Absolute Quantification of Matrix Metabolites Reveals the Dynamics of Mitochondrial Metabolism

Cell

Volumn 166, Issue 5, 2016, Pages 1324-1337.e11

  Chen, Walter W ^a,b,c   Freinkman, Elizaveta ^a   Wang, Tim ^a,b,c   Birsoy, Kıvanç ^d   Sabatini, David M ^a,b,c  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c KOCH INSTITUTE FOR INTEGRATIVE CANCER RESEARCH   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; CELL COMPARTMENTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSOL; EXTRACELLULAR MATRIX; HUMAN; METABOLITE; MITOCHONDRIAL RESPIRATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RESPIRATORY CHAIN; ELECTRON TRANSPORT; GENETICS; HELA CELL LINE; METABOLISM; METABOLOME; MITOCHONDRION;

ELECTRON TRANSPORT; HELA CELLS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; MITOCHONDRIA; PYRUVIC ACID;

EID: 84983792422     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.07.040     Document Type: Article

References (48)

1. Berry, M.N., Barritt, G.J., Edwards, A.M., Burdon, R.H., Isolated Hepatocytes: Preparation, Properties and Applications: Preparation, Properties and Applications. 1991, Elsevier.
2. Berthet, J., Baudhuin, P., A remark about the determination of the water content of mitochondria. J. Cell Biol. 34 (1967), 701–702.
3. Bestwick, R.K., Moffett, G.L., Mathews, C.K., Selective expansion of mitochondrial nucleoside triphosphate pools in antimetabolite-treated HeLa cells. J. Biol. Chem. 257 (1982), 9300–9304.
4. Birsoy, K., Wang, T., Chen, W.W., Freinkman, E., Abu-Remaileh, M., Sabatini, D.M., An essential role of the mitochondrial electron transport chain in cell proliferation is to enable aspartate synthesis. Cell 162 (2015), 540–551.
5. Bogenhagen, D., Clayton, D.A., The number of mitochondrial deoxyribonucleic acid genomes in mouse L and human HeLa cells. Quantitative isolation of mitochondrial deoxyribonucleic acid. J. Biol. Chem. 249 (1974), 7991–7995.
6. Bowsher, C.G., Tobin, A.K., Compartmentation of metabolism within mitochondria and plastids. J. Exp. Bot. 52 (2001), 513–527.
7. Cacciatore, S., Loda, M., Innovation in metabolomics to improve personalized healthcare. Ann. N Y Acad. Sci. 1346 (2015), 57–62.
8. Cardaci, S., Zheng, L., MacKay, G., van den Broek, N.J.F., MacKenzie, E.D., Nixon, C., Stevenson, D., Tumanov, S., Bulusu, V., Kamphorst, J.J., et al. Pyruvate carboxylation enables growth of SDH-deficient cells by supporting aspartate biosynthesis. Nat. Cell Biol. 17 (2015), 1317–1326.
9. Chantranupong, L., Wolfson, R.L., Orozco, J.M., Saxton, R.A., Scaria, S.M., Bar-Peled, L., Spooner, E., Isasa, M., Gygi, S.P., Sabatini, D.M., The Sestrins interact with GATOR2 to negatively regulate the amino-acid-sensing pathway upstream of mTORC1. Cell Rep. 9 (2014), 1–8.
10. Chen, W.W., Birsoy, K., Mihaylova, M.M., Snitkin, H., Stasinski, I., Yucel, B., Bayraktar, E.C., Carette, J.E., Clish, C.B., Brummelkamp, T.R., et al. Inhibition of ATPIF1 ameliorates severe mitochondrial respiratory chain dysfunction in mammalian cells. Cell Rep. 7 (2014), 27–34.
11. Corcelli, A., Saponetti, M.S., Zaccagnino, P., Lopalco, P., Mastrodonato, M., Liquori, G.E., Lorusso, M., Mitochondria isolated in nearly isotonic KCl buffer: Focus on cardiolipin and organelle morphology. Biochim. Biophys. Acta 1798 (2010), 681–687.
12. Elo, J.M., Yadavalli, S.S., Euro, L., Isohanni, P., Götz, A., Carroll, C.J., Valanne, L., Alkuraya, F.S., Uusimaa, J., Paetau, A., et al. Mitochondrial phenylalanyl-tRNA synthetase mutations underlie fatal infantile Alpers encephalopathy. Hum. Mol. Genet. 21 (2012), 4521–4529.
13. Erecińska, M., Wilson, D.F., Nishiki, K., Homeostatic regulation of cellular energy metabolism: experimental characterization in vivo and fit to a model. Am. J. Physiol. 234 (1978), C82–C89.
14. Fly, R., Lloyd, J., Krueger, S., Fernie, A., Merwe, M.J., Improvements to define mitochondrial metabolomics using nonaqueous fractionation. Whelan, J., Murcha, W.M., (eds.) Plant Mitochondria: Methods and Protocols, 2015, Springer, 197–210.
15. Gerencser, A.A., Chinopoulos, C., Birket, M.J., Jastroch, M., Vitelli, C., Nicholls, D.G., Brand, M.D., Quantitative measurement of mitochondrial membrane potential in cultured cells: calcium-induced de- and hyperpolarization of neuronal mitochondria. J. Physiol. 590 (2012), 2845–2871.
16. Harris, M., Pyruvate blocks expression of sensitivity to antimycin A and chloramphenicol. Somatic Cell Genet. 6 (1980), 699–708.
17. Idell-Wenger, J.A., Grotyohann, L.W., Neely, J.R., Coenzyme A and carnitine distribution in normal and ischemic hearts. J. Biol. Chem. 253 (1978), 4310–4318.
18. Kanehisa, M., Goto, S., KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28 (2000), 27–30.
19. Ke, H., Lewis, I.A., Morrisey, J.M., McLean, K.J., Ganesan, S.M., Painter, H.J., Mather, M.W., Jacobs-Lorena, M., Llinás, M., Vaidya, A.B., Genetic investigation of tricarboxylic acid metabolism during the Plasmodium falciparum life cycle. Cell Rep. 11 (2015), 164–174.
20. King, M.P., Attardi, G., Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246 (1989), 500–503.
21. Linskens, H.F., Anderson, J.M., Anderson, B., Jackson, J.F., Berkowitz, G.A., Cline, K., Gibbs, M., Goldberg, R., Hirokawa, T., Huang, A.H.C., Cell Components. 2012, Springer.
22. Markovitz, P.J., Chuang, D.T., Cox, R.P., Familial hyperlysinemias. Purification and characterization of the bifunctional aminoadipic semialdehyde synthase with lysine-ketoglutarate reductase and saccharopine dehydrogenase activities. J. Biol. Chem. 259 (1984), 11643–11646.
23. Matuszczyk, J.-C., Teleki, A., Pfizenmaier, J., Takors, R., Compartment-specific metabolomics for CHO reveals that ATP pools in mitochondria are much lower than in cytosol. Biotechnol. J. 10 (2015), 1639–1650.
24. Messmer, M., Blais, S.P., Balg, C., Chênevert, R., Grenier, L., Lagüe, P., Sauter, C., Sissler, M., Giegé, R., Lapointe, J., Florentz, C., Peculiar inhibition of human mitochondrial aspartyl-tRNA synthetase by adenylate analogs. Biochimie 91 (2009), 596–603.
25. Mullen, A.R., Wheaton, W.W., Jin, E.S., Chen, P.-H., Sullivan, L.B., Cheng, T., Yang, Y., Linehan, W.M., Chandel, N.S., DeBerardinis, R.J., Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 481 (2012), 385–388.
26. Nemoto, Y., De Camilli, P., Recruitment of an alternatively spliced form of synaptojanin 2 to mitochondria by the interaction with the PDZ domain of a mitochondrial outer membrane protein. EMBO J. 18 (1999), 2991–3006.
27. Nishiki, K., Erecińska, M., Wilson, D.F., Energy relationships between cytosolic metabolism and mitochondrial respiration in rat heart. Am. J. Physiol. 234 (1978), C73–C81.
28. Pagliarini, D.J., Calvo, S.E., Chang, B., Sheth, S.A., Vafai, S.B., Ong, S.-E., Walford, G.A., Sugiana, C., Boneh, A., Chen, W.K., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134 (2008), 112–123.
29. Palmieri, F., The mitochondrial transporter family SLC25: identification, properties and physiopathology. Mol. Aspects Med. 34 (2013), 465–484.
30. Roede, J.R., Park, Y., Li, S., Strobel, F.H., Jones, D.P., Detailed mitochondrial phenotyping by high resolution metabolomics. PLoS ONE, 7, 2012, e33020.
31. Ross-Inta, C., Tsai, C.-Y., Giulivi, C., The mitochondrial pool of free amino acids reflects the composition of mitochondrial DNA-encoded proteins: indication of a post- translational quality control for protein synthesis. Biosci. Rep. 28 (2008), 239–249.
32. Safer, B., The metabolic significance of the malate-aspartate cycle in heart. Circ. Res. 37 (1975), 527–533.
33. Saldanha, A.J., Java Treeview—extensible visualization of microarray data. Bioinformatics 20 (2004), 3246–3248.
34. Scovassi, A.I., Mitochondrial poly(ADP-ribosylation): from old data to new perspectives. FASEB J. 18 (2004), 1487–1488.
35. Shaham, O., Slate, N.G., Goldberger, O., Xu, Q., Ramanathan, A., Souza, A.L., Clish, C.B., Sims, K.B., Mootha, V.K., A plasma signature of human mitochondrial disease revealed through metabolic profiling of spent media from cultured muscle cells. Proc. Natl. Acad. Sci. USA 107 (2010), 1571–1575.
36. Srere, P.A., Sumegi, B., Organization of the mitochondrial matrix. Brautbar, N., Boston, M.A., (eds.) Myocardial and Skeletal Muscle Bioenergetics, 1986, Springer, 13–25.
37. Stark, R., Pasquel, F., Turcu, A., Pongratz, R.L., Roden, M., Cline, G.W., Shulman, G.I., Kibbey, R.G., Phosphoenolpyruvate cycling via mitochondrial phosphoenolpyruvate carboxykinase links anaplerosis and mitochondrial GTP with insulin secretion. J. Biol. Chem. 284 (2009), 26578–26590.
38. Stark, R., Guebre-Egziabher, F., Zhao, X., Feriod, C., Dong, J., Alves, T.C., Ioja, S., Pongratz, R.L., Bhanot, S., Roden, M., et al. A role for mitochondrial phosphoenolpyruvate carboxykinase (PEPCK-M) in the regulation of hepatic gluconeogenesis. J. Biol. Chem. 289 (2014), 7257–7263.
39. Sullivan, L.B., Gui, D.Y., Hosios, A.M., Bush, L.N., Freinkman, E., Vander Heiden, M.G., Supporting aspartate biosynthesis is an essential function of respiration in proliferating cells. Cell 162 (2015), 552–563.
40. Tischler, M.E., Hecht, P., Williamson, J.R., Determination of mitochondrial/cytosolic metabolite gradients in isolated rat liver cells by cell disruption. Arch. Biochem. Biophys. 181 (1977), 278–293.
41. Van Vranken, J.G., Rutter, J., You down with ETC? Yeah, you know D!. Cell 162 (2015), 471–473.
42. Vianey-Liaud, C., Divry, P., Gregersen, N., Mathieu, M., The inborn errors of mitochondrial fatty acid oxidation. J. Inherit. Metab. Dis. 10:Suppl 1 (1987), 159–200.
43. ε-succinylation of proteins in the chemical conditions of the mitochondrial matrix. J. Biol. Chem. 288 (2013), 29036–29045.
44. Wallace, D.C., A mitochondrial bioenergetic etiology of disease. J. Clin. Invest. 123 (2013), 1405–1412.
45. Wheaton, W.W., Weinberg, S.E., Hamanaka, R.B., Soberanes, S., Sullivan, L.B., Anso, E., Glasauer, A., Dufour, E., Mutlu, G.M., Budigner, G.S., Chandel, N.S., Metformin inhibits mitochondrial complex I of cancer cells to reduce tumorigenesis. eLife, 3, 2014, e02242.
46. Wiegand, G., Remington, S.J., Citrate synthase: structure, control, and mechanism. Annu. Rev. Biophys. Biophys. Chem. 15 (1986), 97–117.
47. Williamson, J.R., Corkey, B.E., Assay of citric acid cycle intermediates and related compounds—Update with tissue metabolite levels and intracellular distribution. Methods in Enzymology, 1979, Academic Press, 200–222.
48. Yoshii, S.R., Kishi, C., Ishihara, N., Mizushima, N., Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J. Biol. Chem. 286 (2011), 19630–19640.