An Essential Role of the Mitochondrial Electron Transport Chain in Cell Proliferation Is to Enable Aspartate Synthesis

Cell

Volumn 162, Issue 3, 2015, Pages 540-551

  Birsoy, Kivanç ^a,b,c,d   Wang, Tim ^a,b,c   Chen, Walter W ^a,b,c   Freinkman, Elizaveta ^a   Abu Remaileh, Monther ^a,b,c   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

ASPARTATE AMINOTRANSFERASE; ASPARTIC ACID; MITOCHONDRIAL DNA; PHENFORMIN; PYRUVIC ACID; ASPARTATE AMINOTRANSFERASE ISOENZYME 1;

AEROBIC METABOLISM; ARTICLE; CELL PROLIFERATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CYBRID; CYTOSOL; ELECTRON TRANSPORT; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; JURKAT CELL LINE; MITOCHONDRION; OXIDATION REDUCTION STATE; OXYGEN CONSUMPTION; PLEIOTROPY; PRIORITY JOURNAL; RESPIRATORY CHAIN; SUPPLEMENTATION; SYNTHESIS; BIOSYNTHESIS; GENETICS; METABOLISM; MUTATION;

ASPARTATE AMINOTRANSFERASE, CYTOPLASMIC; ASPARTIC ACID; CELL PROLIFERATION; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT; HUMANS; JURKAT CELLS; MITOCHONDRIA; MUTATION; PHENFORMIN; PYRUVIC ACID;

EID: 84938232611     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.07.016     Document Type: Article

References (56)

1. J. Barretina, G. Caponigro, N. Stransky, K. Venkatesan, A.A. Margolin, S. Kim, C.J. Wilson, J. Lehár, G.V. Kryukov, D. Sonkin, and et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity Nature 483 2012 603 607
2. E.L. Bell, T.A. Klimova, J. Eisenbart, C.T. Moraes, M.P. Murphy, G.R. Budinger, and N.S. Chandel The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production J. Cell Biol. 177 2007 1029 1036
3. A. Bender, K.J. Krishnan, C.M. Morris, G.A. Taylor, A.K. Reeve, R.H. Perry, E. Jaros, J.S. Hersheson, J. Betts, T. Klopstock, and et al. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease Nat. Genet. 38 2006 515 517
4. K. Birsoy, R. Possemato, F.K. Lorbeer, E.C. Bayraktar, P. Thiru, B. Yucel, T. Wang, W.W. Chen, C.B. Clish, and D.M. Sabatini Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides Nature 508 2014 108 112
5. A. Boveris, N. Oshino, and B. Chance The cellular production of hydrogen peroxide Biochem. J. 128 1972 617 630
6. N.S. Chandel Mitochondria as signaling organelles BMC Biol. 12 2014 34
7. W.W. Chen, K. Birsoy, M.M. Mihaylova, H. Snitkin, I. Stasinski, B. Yucel, E.C. Bayraktar, J.E. Carette, C.B. Clish, T.R. Brummelkamp, and et al. Inhibition of ATPIF1 ameliorates severe mitochondrial respiratory chain dysfunction in mammalian cells Cell Rep. 7 2014 27 34
8. G.T. Consortium GTEx Consortium The Genotype-Tissue Expression (GTEx) project Nat. Genet. 45 2013 580 585
9. I.F. De Coo, W.O. Renier, W. Ruitenbeek, H.J. Ter Laak, M. Bakker, H. Schägger, B.A. Van Oost, and H.J. Smeets A 4-base pair deletion in the mitochondrial cytochrome b gene associated with parkinsonism/MELAS overlap syndrome Ann. Neurol. 45 1999 130 133
10. F. Di Lisa, and M. Ziegler Pathophysiological relevance of mitochondria in NAD(+) metabolism FEBS Lett. 492 2001 4 8
11. S. DiMauro Pathogenesis and treatment of mitochondrial myopathies: recent advances Acta Myol. 29 2010 333 338
12. S.M. Fendt, E.L. Bell, M.A. Keibler, S.M. Davidson, G.J. Wirth, B. Fiske, J.R. Mayers, M. Schwab, G. Bellinger, A. Csibi, and et al. Metformin decreases glucose oxidation and increases the dependency of prostate cancer cells on reductive glutamine metabolism Cancer Res. 73 2013 4429 4438
13. C. Frezza, L. Zheng, O. Folger, K.N. Rajagopalan, E.D. MacKenzie, L. Jerby, M. Micaroni, B. Chaneton, J. Adam, A. Hedley, and et al. Haem oxygenase is synthetically lethal with the tumour suppressor fumarate hydratase Nature 477 2011 225 228
14. T. Fujii, F. Nozaki, K. Saito, A. Hayashi, Y. Nishigaki, K. Murayama, M. Tanaka, Y. Koga, I. Hiejima, and T. Kumada Efficacy of pyruvate therapy in patients with mitochondrial disease: a semi-quantitative clinical evaluation study Mol. Genet. Metab. 112 2014 133 138
15. A. Geissler, T. Krimmer, U. Bömer, B. Guiard, J. Rassow, and N. Pfanner Membrane potential-driven protein import into mitochondria. The sorting sequence of cytochrome b(2) modulates the deltapsi-dependence of translocation of the matrix-targeting sequence Mol. Biol. Cell 11 2000 3977 3991
16. D.R. Green, and J.C. Reed Mitochondria and apoptosis Science 281 1998 1309 1312
17. Y.H. Han, S.H. Kim, S.Z. Kim, and W.H. Park Antimycin A as a mitochondrial electron transport inhibitor prevents the growth of human lung cancer A549 cells Oncol. Rep. 20 2008 689 693
18. A. Hansson, N. Hance, E. Dufour, A. Rantanen, K. Hultenby, D.A. Clayton, R. Wibom, and N.G. Larsson A switch in metabolism precedes increased mitochondrial biogenesis in respiratory chain-deficient mouse hearts Proc. Natl. Acad. Sci. USA 101 2004 3136 3141
19. M. Harris Pyruvate blocks expression of sensitivity to antimycin A and chloramphenicol Somatic Cell Genet. 6 1980 699 708
20. N. Howell, and R. Sager Cytoplasmic genetics of mammalian cells: conditional sensitivity to mitochondrial inhibitors and isolation of new mutant phenotypes Somatic Cell Genet. 5 1979 833 845
21. K. Ishikawa, K. Takenaga, M. Akimoto, N. Koshikawa, A. Yamaguchi, H. Imanishi, K. Nakada, Y. Honma, and J. Hayashi ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis Science 320 2008 661 664
22. M.P. King, and G. Attardi Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation Science 246 1989 500 503
23. M.P. King, and G. Attardi Isolation of human cell lines lacking mitochondrial DNA Methods Enzymol. 264 1996 304 313
24. H. Kokotas, M.B. Petersen, and P.J. Willems Mitochondrial deafness Clin. Genet. 71 2007 379 391
25. W.J. Koopman, P.H. Willems, and J.A. Smeitink Monogenic mitochondrial disorders N. Engl. J. Med. 366 2012 1132 1141
26. R.J. Kulmacz Concerted loss of cyclooxygenase and peroxidase activities from prostaglandin H synthase upon proteolytic attack Prostaglandins 38 1989 277 288
27. A.N. Lane, and T.W. Fan Regulation of mammalian nucleotide metabolism and biosynthesis Nucleic Acids Res. 43 2015 2466 2485
28. M. Löffler, J. Jöckel, G. Schuster, and C. Becker Dihydroorotat-ubiquinone oxidoreductase links mitochondria in the biosynthesis of pyrimidine nucleotides Mol. Cell. Biochem. 174 1997 125 129
29. C.M. Metallo, P.A. Gameiro, E.L. Bell, K.R. Mattaini, J. Yang, K. Hiller, C.M. Jewell, Z.R. Johnson, D.J. Irvine, L. Guarente, and et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia Nature 481 2012 380 384
30. P. Mitchell Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism Nature 191 1961 144 148
31. A.R. Mullen, W.W. Wheaton, E.S. Jin, P.H. Chen, L.B. Sullivan, T. Cheng, Y. Yang, W.M. Linehan, N.S. Chandel, and R.J. DeBerardinis Reductive carboxylation supports growth in tumour cells with defective mitochondria Nature 481 2012 385 388
32. C.B. Newgard, J. An, J.R. Bain, M.J. Muehlbauer, R.D. Stevens, L.F. Lien, A.M. Haqq, S.H. Shah, M. Arlotto, C.A. Slentz, and et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance Cell Metab. 9 2009 311 326
33. D.G. Nicholls, and S.L. Budd Mitochondria and neuronal survival Physiol. Rev. 80 2000 315 360
34. M.R. Owen, E. Doran, and A.P. Halestrap Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain Biochem. J. 348 2000 607 614
35. D.J. Pagliarini, and J. Rutter Hallmarks of a new era in mitochondrial biochemistry Genes Dev. 27 2013 2615 2627
36. J.A. Petros, A.K. Baumann, E. Ruiz-Pesini, M.B. Amin, C.Q. Sun, J. Hall, S. Lim, M.M. Issa, W.D. Flanders, S.H. Hosseini, and et al. mtDNA mutations increase tumorigenicity in prostate cancer Proc. Natl. Acad. Sci. USA 102 2005 719 724
37. G. Pfeffer, K. Majamaa, D.M. Turnbull, D. Thorburn, and P.F. Chinnery Treatment for mitochondrial disorders Cochrane Database Syst. Rev. 4 2012 CD004426
38. N. Raimundo, L. Song, T.E. Shutt, S.E. McKay, J. Cotney, M.X. Guan, T.C. Gilliland, D. Hohuan, J. Santos-Sacchi, and G.S. Shadel Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness Cell 148 2012 716 726
39. M. Rana, I. de Coo, F. Diaz, H. Smeets, and C.T. Moraes An out-of-frame cytochrome b gene deletion from a patient with parkinsonism is associated with impaired complex III assembly and an increase in free radical production Ann. Neurol. 48 2000 774 781
40. B. Safer The Metabolic Significance of the Malate-Aspartate Cycle in Heart Circ. Res. 37 1975 527 533
41. K. Saito, N. Kimura, N. Oda, H. Shimomura, T. Kumada, T. Miyajima, K. Murayama, M. Tanaka, and T. Fujii Pyruvate therapy for mitochondrial DNA depletion syndrome Biochim. Biophys. Acta 1820 2012 632 636
42. A.F. Santidrian, A. Matsuno-Yagi, M. Ritland, B.B. Seo, S.E. LeBoeuf, L.J. Gay, T. Yagi, and B. Felding-Habermann Mitochondrial complex I activity and NAD+/NADH balance regulate breast cancer progression J. Clin. Invest. 123 2013 1068 1081
43. E.A. Schon, S. DiMauro, and M. Hirano Human mitochondrial DNA: roles of inherited and somatic mutations Nat. Rev. Genet. 13 2012 878 890
44. J. Son, C.A. Lyssiotis, H. Ying, X. Wang, S. Hua, M. Ligorio, R.M. Perera, C.R. Ferrone, E. Mullarky, N. Shyh-Chang, and et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway Nature 496 2013 101 105
45. L.R. Stein, and S. Imai The dynamic regulation of NAD metabolism in mitochondria Trends Endocrinol. Metab. 23 2012 420 428
46. T. Storck, S. Schulte, K. Hofmann, and W. Stoffel Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain Proc. Natl. Acad. Sci. USA 89 1992 10955 10959
47. L.B. Sullivan, D.Y. Gui, A.M. Hosios, L.N. Bush, E. Freinkman, and M.G. Vander Heiden Supporting Aspartate Biosynthesis Is an Essential Function of Respiration in Proliferating Cells Cell 162 2015 552 563 this issue
48. R.H. Swerdlow, J.K. Parks, S.W. Miller, J.B. Tuttle, P.A. Trimmer, J.P. Sheehan, J.P. Bennett Jr., R.E. Davis, and W.D. Parker Jr. Origin and functional consequences of the complex I defect in Parkinson's disease Ann. Neurol. 40 1996 663 671
49. M.D. Toney Aspartate aminotransferase: an old dog teaches new tricks Arch. Biochem. Biophys. 544 2014 119 127
50. D.C. Wallace Mitochondrial diseases in man and mouse Science 283 1999 1482 1488
51. D.C. Wallace A mitochondrial bioenergetic etiology of disease J. Clin. Invest. 123 2013 1405 1412
52. D.C. Wallace, X.X. Zheng, M.T. Lott, J.M. Shoffner, J.A. Hodge, R.I. Kelley, C.M. Epstein, and L.C. Hopkins Familial mitochondrial encephalomyopathy (MERRF): genetic, pathophysiological, and biochemical characterization of a mitochondrial DNA disease Cell 55 1988 601 610
53. T. Wang, J.J. Wei, D.M. Sabatini, and E.S. Lander Genetic screens in human cells using the CRISPR-Cas9 system Science 343 2014 80 84
54. W.W. Wheaton, S.E. Weinberg, R.B. Hamanaka, S. Soberanes, L.B. Sullivan, E. Anso, A. Glasauer, E. Dufour, G.M. Mutlu, G.S. Budigner, and N.S. Chandel Metformin inhibits mitochondrial complex I of cancer cells to reduce tumorigenesis eLife 3 2014 e02242
55. H.M. Wilkins, S.M. Carl, and R.H. Swerdlow Cytoplasmic hybrid (cybrid) cell lines as a practical model for mitochondriopathies Redox biol. 2 2014 619 631
56. J.A. Wuu, L.Y. Wen, T.Y. Chuang, and G.G. Chang Amino acid concentrations in serum and aqueous humor from subjects with extreme myopia or senile cataract Clin. Chem. 34 1988 1610 1613