Differential Glutamate Metabolism in Proliferating and Quiescent Mammary Epithelial Cells

Cell Metabolism

Volumn 23, Issue 5, 2016, Pages 867-880

  Coloff, Jonathan L ^a   Murphy, J Patrick ^a   Braun, Craig R ^a   Harris, Isaac S ^a   Shelton, Laura M ^b   Kami, Kenjiro ^b   Gygi, Steven P ^a   Selfors, Laura M ^a   Brugge, Joan S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Keio University and Human Metabolome Technologies Inc   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINOTRANSFERASE; ASPARTIC ACID; CARBON; EPIDERMAL GROWTH FACTOR; GLUTAMATE DEHYDROGENASE; INSULIN; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR NRF2; TRICARBOXYLIC ACID; GLUTAMIC ACID; NITROGEN; TARGET OF RAPAMYCIN KINASE;

ACID SECRETION; ARTICLE; BIOSYNTHESIS; BREAST CANCER; BREAST EPITHELIUM CELL; CARBON METABOLISM; CELL PROLIFERATION; GENE EXPRESSION; GLUCOSE INTAKE; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INSULIN BLOOD LEVEL; NITROGEN METABOLISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TRANSAMINATION; BIOLOGICAL MODEL; BREAST TUMOR; CELL CULTURE; CYTOLOGY; ENZYMOLOGY; EPITHELIUM CELL; FEMALE; MAMMARY GLAND; METABOLISM; METABOLOMICS; PATHOLOGY; PROTEOMICS;

BREAST NEOPLASMS; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; GLUTAMATE DEHYDROGENASE; GLUTAMIC ACID; HUMANS; MAMMARY GLANDS, HUMAN; METABOLOMICS; MODELS, BIOLOGICAL; NITROGEN ISOTOPES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSAMINASES;

EID: 84964619842     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.03.016     Document Type: Article

References (58)

1. C.M. Adams Role of the transcription factor ATF4 in the anabolic actions of insulin and the anti-anabolic actions of glucocorticoids J. Biol. Chem. 282 2007 16744 16753
2. D.E. Atkinson The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers Biochemistry 7 1968 4030 4034
3. K. Birsoy, T. Wang, W.W. Chen, E. Freinkman, M. Abu-Remaileh, and D.M. Sabatini An essential role of the mitochondrial electron transport chain in cell proliferation is to enable aspartate synthesis Cell 162 2015 540 551
4. M.J. Brauer, A.J. Saldanha, K. Dolinski, and D. Botstein Homeostatic adjustment and metabolic remodeling in glucose-limited yeast cultures Mol. Biol. Cell 16 2005 2503 2517
5. S. Cardaci, L. Zheng, G. MacKay, N.J. van den Broek, E.D. MacKenzie, C. Nixon, D. Stevenson, S. Tumanov, V. Bulusu, J.J. Kamphorst, and et al. Pyruvate carboxylation enables growth of SDH-deficient cells by supporting aspartate biosynthesis Nat. Cell Biol. 17 2015 1317 1326
6. H.A. Coller Cell biology. The essence of quiescence Science 334 2011 1074 1075
7. A. Csibi, S.M. Fendt, C. Li, G. Poulogiannis, A.Y. Choo, D.J. Chapski, S.M. Jeong, J.M. Dempsey, A. Parkhitko, T. Morrison, and et al. The mTORC1 pathway stimulates glutamine metabolism and cell proliferation by repressing SIRT4 Cell 153 2013 840 854
8. A. Csibi, G. Lee, S.O. Yoon, H. Tong, D. Ilter, I. Elia, S.M. Fendt, T.M. Roberts, and J. Blenis The mTORC1/S6K1 pathway regulates glutamine metabolism through the eIF4B-dependent control of c-Myc translation Curr. Biol. 24 2014 2274 2280
9. R.J. DeBerardinis, A. Mancuso, E. Daikhin, I. Nissim, M. Yudkoff, S. Wehrli, and C.B. Thompson Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis Proc. Natl. Acad. Sci. USA 104 2007 19345 19350
10. J. Debnath, and J.S. Brugge Modelling glandular epithelial cancers in three-dimensional cultures Nat. Rev. Cancer 5 2005 675 688
11. G.M. DeNicola, P.H. Chen, E. Mullarky, J.A. Sudderth, Z. Hu, D. Wu, H. Tang, Y. Xie, J.M. Asara, K.E. Huffman, and et al. NRF2 regulates serine biosynthesis in non-small cell lung cancer Nat. Genet. 47 2015 1475 1481
12. C.C. Dibble, and B.D. Manning Signal integration by mTORC1 coordinates nutrient input with biosynthetic output Nat. Cell Biol. 15 2013 555 564
13. D.R. Fernandez, T. Telarico, E. Bonilla, Q. Li, S. Banerjee, F.A. Middleton, P.E. Phillips, M.K. Crow, S. Oess, W. Muller-Esterl, and A. Perl Activation of mammalian target of rapamycin controls the loss of TCRzeta in lupus T cells through HRES-1/Rab4-regulated lysosomal degradation J. Immunol. 182 2009 2063 2073
14. D.C. Fingar, C.J. Richardson, A.R. Tee, L. Cheatham, C. Tsou, and J. Blenis mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E Mol. Cell. Biol. 24 2004 200 216
15. K.A. Frauwirth, J.L. Riley, M.H. Harris, R.V. Parry, J.C. Rathmell, D.R. Plas, R.L. Elstrom, C.H. June, and C.B. Thompson The CD28 signaling pathway regulates glucose metabolism Immunity 16 2002 769 777
16. P. Gao, I. Tchernyshyov, T.C. Chang, Y.S. Lee, K. Kita, T. Ochi, K.I. Zeller, A.M. De Marzo, J.E. Van Eyk, J.T. Mendell, and C.V. Dang c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism Nature 458 2009 762 765
17. M.L. Gatza, G.O. Silva, J.S. Parker, C. Fan, and C.M. Perou An integrated genomics approach identifies drivers of proliferation in luminal-subtype human breast cancer Nat. Genet. 46 2014 1051 1059
18. C.R. Green, M. Wallace, A.S. Divakaruni, S.A. Phillips, A.N. Murphy, T.P. Ciaraldi, and C.M. Metallo Branched-chain amino acid catabolism fuels adipocyte differentiation and lipogenesis Nat. Chem. Biol. 12 2016 15 21
19. M.C. Haigis, R. Mostoslavsky, K.M. Haigis, K. Fahie, D.C. Christodoulou, A.J. Murphy, D.M. Valenzuela, G.D. Yancopoulos, M. Karow, G. Blander, and et al. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells Cell 126 2006 941 954
20. J. Han, S.H. Back, J. Hur, Y.H. Lin, R. Gildersleeve, J. Shan, C.L. Yuan, D. Krokowski, S. Wang, M. Hatzoglou, and et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death Nat. Cell Biol. 15 2013 481 490
21. C.T. Hensley, A.T. Wasti, and R.J. DeBerardinis Glutamine and cancer: cell biology, physiology, and clinical opportunities J. Clin. Invest. 123 2013 3678 3684
22. K. Hiller, C.M. Metallo, J.K. Kelleher, and G. Stephanopoulos Nontargeted elucidation of metabolic pathways using stable-isotope tracers and mass spectrometry Anal. Chem. 82 2010 6621 6628
23. L. Jin, D. Li, G.N. Alesi, J. Fan, H.B. Kang, Z. Lu, T.J. Boggon, P. Jin, H. Yi, E.R. Wright, and et al. Glutamate dehydrogenase 1 signals through antioxidant glutathione peroxidase 1 to regulate redox homeostasis and tumor growth Cancer Cell 27 2015 257 270
24. P. Korangath, W.W. Teo, H. Sadik, L. Han, N. Mori, C.M. Huijts, F. Wildes, S. Bharti, Z. Zhang, C.A. Santa-Maria, and et al. Targeting glutamine metabolism in breast cancer with aminooxyacetate Clin. Cancer Res. 21 2015 3263 3273
25. H. Kouros-Mehr, E.M. Slorach, M.D. Sternlicht, and Z. Werb GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland Cell 127 2006 1041 1055
26. J.M. Lemons, X.J. Feng, B.D. Bennett, A. Legesse-Miller, E.L. Johnson, I. Raitman, E.A. Pollina, H.A. Rabitz, J.D. Rabinowitz, and H.A. Coller Quiescent fibroblasts exhibit high metabolic activity PLoS Biol. 8 2010 e1000514
27. C.T. Leung, and J.S. Brugge Outgrowth of single oncogene-expressing cells from suppressive epithelial environments Nature 482 2012 410 413
28. M. Li, C. Li, A. Allen, C.A. Stanley, and T.J. Smith The structure and allosteric regulation of glutamate dehydrogenase Neurochem. Int. 59 2011 445 455
29. J.W. Locasale, A.R. Grassian, T. Melman, C.A. Lyssiotis, K.R. Mattaini, A.J. Bass, G. Heffron, C.M. Metallo, T. Muranen, H. Sharfi, and et al. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis Nat. Genet. 43 2011 869 874
30. S.Y. Lunt, and M.G. Vander Heiden Aerobic glycolysis: meeting the metabolic requirements of cell proliferation Annu. Rev. Cell Dev. Biol. 27 2011 441 464
31. Z. Ma, and K. Vosseller O-GlcNAc in cancer biology Amino Acids 45 2013 719 733
32. N.J. Maciver, S.R. Jacobs, H.L. Wieman, J.A. Wofford, J.L. Coloff, and J.C. Rathmell Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival J. Leukoc. Biol. 84 2008 949 957
33. A.I. McClatchey, and A.S. Yap Contact inhibition (of proliferation) redux Curr. Opin. Cell Biol. 24 2012 685 694
34. M. Meng, S. Chen, T. Lao, D. Liang, and N. Sang Nitrogen anabolism underlies the importance of glutaminolysis in proliferating cells Cell Cycle 9 2010 3921 3932
35. M.A. Merritt, S. Bentink, M. Schwede, M.P. Iwanicki, J. Quackenbush, T. Woo, E.S. Agoston, F. Reinhardt, C.P. Crum, R.S. Berkowitz, and et al. Gene expression signature of normal cell-of-origin predicts ovarian tumor outcomes PLoS ONE 8 2013 e80314
36. Y. Mitsuishi, K. Taguchi, Y. Kawatani, T. Shibata, T. Nukiwa, H. Aburatani, M. Yamamoto, and H. Motohashi Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming Cancer Cell 22 2012 66 79
37. J.P. Murphy, R.A. Everley, J.L. Coloff, and S.P. Gygi Combining amine metabolomics and quantitative proteomics of cancer cells using derivatization with isobaric tags Anal. Chem. 86 2014 3585 3593
38. J.P. Murphy, E. Stepanova, R.A. Everley, J.A. Paulo, and S.P. Gygi Comprehensive temporal protein dynamics during the diauxic shift in Saccharomyces cerevisiae Mol. Cell. Proteomics 14 2015 2454 2465
39. B.N. Nicolay, P.A. Gameiro, K. Tschöp, M. Korenjak, A.M. Heilmann, J.M. Asara, G. Stephanopoulos, O. Iliopoulos, and N.J. Dyson Loss of RBF1 changes glutamine catabolism Genes Dev. 27 2013 182 196
40. T.O. Nielsen, J.S. Parker, S. Leung, D. Voduc, M. Ebbert, T. Vickery, S.R. Davies, J. Snider, I.J. Stijleman, J. Reed, and et al. A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer Clin. Cancer Res. 16 2010 5222 5232
41. R. Possemato, K.M. Marks, Y.D. Shaul, M.E. Pacold, D. Kim, K. Birsoy, S. Sethumadhavan, H.K. Woo, H.G. Jang, A.K. Jha, and et al. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer Nature 476 2011 346 350
42. G. Qing, B. Li, A. Vu, N. Skuli, Z.E. Walton, X. Liu, P.A. Mayes, D.R. Wise, C.B. Thompson, J.M. Maris, and et al. ATF4 regulates MYC-mediated neuroblastoma cell death upon glutamine deprivation Cancer Cell 22 2012 631 644
43. J.C. Rathmell, C.J. Fox, D.R. Plas, P.S. Hammerman, R.M. Cinalli, and C.B. Thompson Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival Mol. Cell. Biol. 23 2003 7315 7328
44. Z.T. Schafer, A.R. Grassian, L. Song, Z. Jiang, Z. Gerhart-Hines, H.Y. Irie, S. Gao, P. Puigserver, and J.S. Brugge Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment Nature 461 2009 109 113
45. P. Shashidharan, T.M. Michaelidis, N.K. Robakis, A. Kresovali, J. Papamatheakis, and A. Plaitakis Novel human glutamate dehydrogenase expressed in neural and testicular tissues and encoded by an X-linked intronless gene J. Biol. Chem. 269 1994 16971 16976
46. 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
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
48. I. Thiele, N. Swainston, R.M. Fleming, A. Hoppe, S. Sahoo, M.K. Aurich, H. Haraldsdottir, M.L. Mo, O. Rolfsson, M.D. Stobbe, and et al. A community-driven global reconstruction of human metabolism Nat. Biotechnol. 31 2013 419 425
49. J.M. Thornburg, K.K. Nelson, B.F. Clem, A.N. Lane, S. Arumugam, A. Simmons, J.W. Eaton, S. Telang, and J. Chesney Targeting aspartate aminotransferase in breast cancer Breast Cancer Res. 10 2008 R84
50. M.G. Vander Heiden, L.C. Cantley, and C.B. Thompson Understanding the Warburg effect: the metabolic requirements of cell proliferation Science 324 2009 1029 1033
51. D. Venet, J.E. Dumont, and V. Detours Most random gene expression signatures are significantly associated with breast cancer outcome PLoS Comput. Biol. 7 2011 e1002240
52. B. Weigelt, and M.J. Bissell Unraveling the microenvironmental influences on the normal mammary gland and breast cancer Semin. Cancer Biol. 18 2008 311 321
53. D.R. Wise, R.J. DeBerardinis, A. Mancuso, N. Sayed, X.Y. Zhang, H.K. Pfeiffer, I. Nissim, E. Daikhin, M. Yudkoff, S.B. McMahon, and C.B. Thompson Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction Proc. Natl. Acad. Sci. USA 105 2008 18782 18787
54. D.T. Worster, T. Schmelzle, N.L. Solimini, E.S. Lightcap, B. Millard, G.B. Mills, J.S. Brugge, and J.G. Albeck Akt and ERK control the proliferative response of mammary epithelial cells to the growth factors IGF-1 and EGF through the cell cycle inhibitor p57Kip2 Sci. Signal. 5 2012 ra19
55. K.M. Yamada, and E. Cukierman Modeling tissue morphogenesis and cancer in 3D Cell 130 2007 601 610
56. C. Yang, J. Sudderth, T. Dang, R.M. Bachoo, J.G. McDonald, and R.J. DeBerardinis Glioblastoma cells require glutamate dehydrogenase to survive impairments of glucose metabolism or Akt signaling Cancer Res. 69 2009 7986 7993
57. C. Yang, B. Ko, C.T. Hensley, L. Jiang, A.T. Wasti, J. Kim, J. Sudderth, M.A. Calvaruso, L. Lumata, M. Mitsche, and et al. Glutamine oxidation maintains the TCA cycle and cell survival during impaired mitochondrial pyruvate transport Mol. Cell 56 2014 414 424
58. A. Zetterberg, and W. Engström Glutamine and the regulation of DNA replication and cell multiplication in fibroblasts J. Cell. Physiol. 108 1981 365 373