Is cancer a metabolic disease? 9582978472

American Journal of Pathology

Volumn 184, Issue 1, 2014, Pages 4-17

  Coller, Hilary A ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; DICHLOROACETIC ACID; GLUCOSE; GLUCOSE TRANSPORTER 1; GLUTAMINE; ISOENZYME; LACTIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PYRUVATE DEHYDROGENASE KINASE; REACTIVE OXYGEN METABOLITE;

ADAPTATION; ANAEROBIC GLYCOLYSIS; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CARCINOGENESIS; DISEASE ASSOCIATION; DRUG INHIBITION; ENZYME ACTIVITY; FITNESS; GENE OVEREXPRESSION; GLUCOSE INTAKE; HUMAN; LYMPHOCYTE ACTIVATION; METABOLIC DISORDER; NEOPLASM; NONHUMAN; ONCOGENE C MYC; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TUMOR MICROENVIRONMENT;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; NEOPLASMS;

EID: 84890406729     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.07.035     Document Type: Review

References (131)

1. O. Warburg On the origin of cancer cells Science 123 1956 309 314
2. J. Czernin, and M.E. Phelps Positron emission tomography scanning: current and future applications Ann Rev Med 53 2002 89 112
3. M. Kunkel, T.E. Reichert, P. Benz, H.A. Lehr, J.H. Jeong, S. Wieand, P. Bartenstein, W. Wagner, and T.L. Whiteside Overexpression of Glut-1 and increased glucose metabolism in tumors are associated with a poor prognosis in patients with oral squamous cell carcinoma Cancer 97 2003 1015 1024
4. E. Mochiki, H. Kuwano, H. Katoh, T. Asao, N. Oriuchi, and K. Endo Evaluation of 18F-2-deoxy-2-fluoro-D-glucose positron emission tomography for gastric cancer World J Surg 28 2004 247 253
5. D.A. Podoloff, R.H. Advani, C. Allred, A.B. Benson 3rd, E. Brown, H.J. Burstein, R.W. Carlson, R.E. Coleman, M.S. Czuczman, D. Delbeke, S.B. Edge, D.S. Ettinger, F.W. Grannis Jr., B.E. Hillner, J.M. Hoffman, K. Kiel, R. Komaki, S.M. Larson, D.A. Mankoff, K.E. Rosenzweig, J.M. Skibber, J. Yahalom, J.M. Yu, and A.D. Zelenetz NCCN task force report: positron emission tomography (PET)/computed tomography (CT) scanning in cancer J Natl Compr Canc Netw 5 Suppl 1 2007 S1 S22
6. S. Walenta, M. Wetterling, M. Lehrke, G. Schwickert, K. Sundfor, E.K. Rofstad, and W. Mueller-Klieser High lactate levels predict likelihood of metastases, tumor recurrence, and restricted patient survival in human cervical cancers Cancer Res 60 2000 916 921
7. D.M. Brizel, T. Schroeder, R.L. Scher, S. Walenta, R.W. Clough, M.W. Dewhirst, and W. Mueller-Klieser Elevated tumor lactate concentrations predict for an increased risk of metastases in head-and-neck cancer Int J Radiat Oncol Biol Phys 51 2001 349 353
8. G. Schwickert, S. Walenta, K. Sundfor, E.K. Rofstad, and W. Mueller-Klieser Correlation of high lactate levels in human cervical cancer with incidence of metastasis Cancer Res 55 1995 4757 4759
9. B. Altenberg, and K.O. Greulich Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes Genomics 84 2004 1014 1020
10. R.A. Medina, and G.I. Owen Glucose transporters: expression, regulation and cancer Biol Res 35 2002 9 26
11. S.N. Reske, K.G. Grillenberger, G. Glatting, M. Port, M. Hildebrandt, F. Gansauge, and H.G. Beger Overexpression of glucose transporter 1 and increased FDG uptake in pancreatic carcinoma J Nucl Med 38 1997 1344 1348
12. S. Rastogi, S. Banerjee, S. Chellappan, and G.R. Simon Glut-1 antibodies induce growth arrest and apoptosis in human cancer cell lines Cancer Lett 257 2007 244 251
13. O. Keunen, M. Johansson, A. Oudin, M. Sanzey, S.A. Rahim, F. Fack, F. Thorsen, T. Taxt, M. Bartos, R. Jirik, H. Miletic, J. Wang, D. Stieber, L. Stuhr, I. Moen, C.B. Rygh, R. Bjerkvig, and S.P. Niclou Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma Proc Natl Acad Sci U S A 108 2011 3749 3754
14. E.J. Fine, C.J. Segal-Isaacson, R.D. Feinman, S. Herszkopf, M.C. Romano, N. Tomuta, A.F. Bontempo, A. Negassa, and J.A. Sparano Targeting insulin inhibition as a metabolic therapy in advanced cancer: a pilot safety and feasibility dietary trial in 10 patients Nutrition 28 2012 1028 1035
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. S.R. Jacobs, C.E. Herman, N.J. Maciver, J.A. Wofford, H.L. Wieman, J.J. Hammen, and J.C. Rathmell Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways J Immunol 180 2008 4476 4486
17. K. Brand Glutamine and glucose metabolism during thymocyte proliferation: pathways of glutamine and glutamate metabolism Biochem J 228 1985 353 361
18. D.A. Hume, J.L. Radik, E. Ferber, and M.J. Weidemann Aerobic glycolysis and lymphocyte transformation Biochem J 174 1978 703 709
19. A. Le, A.N. Lane, M. Hamaker, S. Bose, A. Gouw, J. Barbi, T. Tsukamoto, C.J. Rojas, B.S. Slusher, H. Zhang, L.J. Zimmerman, D.C. Liebler, R.J. Slebos, P.K. Lorkiewicz, R.M. Higashi, T.W. Fan, and C.V. Dang Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells Cell Metab 15 2012 110 121
20. R.C. Osthus, H. Shim, S. Kim, Q. Li, R. Reddy, M. Mukherjee, Y. Xu, D. Wonsey, L.A. Lee, and C.V. Dang Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc J Biol Chem 275 2000 21797 21800
21. S.P. Mathupala, A. Rempel, and P.L. Pedersen Glucose catabolism in cancer cells: identification and characterization of a marked activation response of the type II hexokinase gene to hypoxic conditions J Biol Chem 276 2001 43407 43412
22. S. Matoba, J.G. Kang, W.D. Patino, A. Wragg, M. Boehm, O. Gavrilova, P.J. Hurley, F. Bunz, and P.M. Hwang p53 Regulates mitochondrial respiration Science 312 2006 1650 1653
23. F. Schwartzenberg-Bar-Yoseph, M. Armoni, and E. Karnieli The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression Cancer Res 64 2004 2627 2633
24. E. Bustamante, and P.L. Pedersen High aerobic glycolysis of rat hepatoma cells in culture: role of mitochondrial hexokinase Proc Natl Acad Sci U S A 74 1977 3735 3739
25. A. Marin-Hernandez, S. Rodriguez-Enriquez, P.A. Vital-Gonzalez, F.L. Flores-Rodriguez, M. Macias-Silva, M. Sosa-Garrocho, and R. Moreno-Sanchez Determining and understanding the control of glycolysis in fast-growth tumor cells: flux control by an over-expressed but strongly product-inhibited hexokinase FEBS J 273 2006 1975 1988
26. A. Wolf, S. Agnihotri, J. Micallef, J. Mukherjee, N. Sabha, R. Cairns, C. Hawkins, and A. Guha Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme J Exp Med 208 2011 313 326
27. V.K. Kalia, S. Prabhakara, and V. Narayanan Modulation of cellular radiation responses by 2-deoxy-D-glucose and other glycolytic inhibitors: implications for cancer therapy J Cancer Res Ther 5 Suppl 1 2009 S57 S60
28. R. Wang, C.P. Dillon, L.Z. Shi, S. Milasta, R. Carter, D. Finkelstein, L.L. McCormick, P. Fitzgerald, H. Chi, J. Munger, and D.R. Green The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation Immunity 35 2011 871 882
29. K. Gottlob, N. Majewski, S. Kennedy, E. Kandel, R.B. Robey, and N. Hay Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase Genes Dev 15 2001 1406 1418
30. J.W. Kim, P. Gao, Y.C. Liu, G.L. Semenza, and C.V. Dang Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1 Mol Cell Biol 27 2007 7381 7393
31. S. Vora, J.P. Halper, and D.M. Knowles Alterations in the activity and isozymic profile of human phosphofructokinase during malignant transformation in vivo and in vitro: transformation- and progression-linked discriminants of malignancy Cancer Res 45 1985 2993 3001
32. W. Yi, P.M. Clark, D.E. Mason, M.C. Keenan, C. Hill, W.A. Goddard 3rd, E.C. Peters, E.M. Driggers, and L.C. Hsieh-Wilson Phosphofructokinase 1 glycosylation regulates cell growth and metabolism Science 337 2012 975 980
33. J. Deprez, D. Vertommen, D.R. Alessi, L. Hue, and M.H. Rider Phosphorylation and activation of heart 6-phosphofructo-2-kinase by protein kinase B and other protein kinases of the insulin signaling cascades J Biol Chem 272 1997 17269 17275
34. T. Atsumi, J. Chesney, C. Metz, L. Leng, S. Donnelly, Z. Makita, R. Mitchell, and R. Bucala High expression of inducible 6-phosphofructo-2-kinase/ fructose-2,6-bisphosphatase (iPFK-2; PFKFB3) in human cancers Cancer Res 62 2002 5881 5887
35. S. Telang, A. Yalcin, A.L. Clem, R. Bucala, A.N. Lane, J.W. Eaton, and J. Chesney Ras transformation requires metabolic control by 6-phosphofructo-2- kinase Oncogene 25 2006 7225 7234
36. B. Clem, S. Telang, A. Clem, A. Yalcin, J. Meier, A. Simmons, M.A. Rasku, S. Arumugam, W.L. Dean, J. Eaton, A. Lane, J.O. Trent, and J. Chesney Small-molecule inhibition of 6-phosphofructo-2-kinase activity suppresses glycolytic flux and tumor growth Mol Cancer Ther 7 2008 110 120
37. S. Telang, B.F. Clem, A.C. Klarer, A.L. Clem, J.O. Trent, R. Bucala, and J. Chesney Small molecule inhibition of 6-phosphofructo-2-kinase suppresses T cell activation J Transl Med 10 2012 95
38. K. Bensaad, A. Tsuruta, M.A. Selak, M.N. Vidal, K. Nakano, R. Bartrons, E. Gottlieb, and K.H. Vousden TIGAR, a p53-inducible regulator of glycolysis and apoptosis Cell 126 2006 107 120
39. H.R. Christofk, M.G. Vander Heiden, M.H. Harris, A. Ramanathan, R.E. Gerszten, R. Wei, M.D. Fleming, S.L. Schreiber, and L.C. Cantley The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth Nature 452 2008 230 233
40. M.S. Goldberg, and P.A. Sharp Pyruvate kinase M2-specific siRNA induces apoptosis and tumor regression J Exp Med 209 2012 217 224
41. D. Anastasiou, Y. Yu, W.J. Israelsen, J.K. Jiang, M.B. Boxer, and B.S. Hong Pyruvate kinase M2 activators promote tetramer formation and suppress tumorigenesis Nat Chem Biol 8 2012 1008
42. S.M. Wigfield, S.C. Winter, A. Giatromanolaki, J. Taylor, M.L. Koukourakis, and A.L. Harris PDK-1 regulates lactate production in hypoxia and is associated with poor prognosis in head and neck squamous cancer Br J Cancer 98 2008 1975 1984
43. T. McFate, A. Mohyeldin, H. Lu, J. Thakar, J. Henriques, N.D. Halim, H. Wu, M.J. Schell, T.M. Tsang, O. Teahan, S. Zhou, J.A. Califano, N.H. Jeoung, R.A. Harris, and A. Verma Pyruvate dehydrogenase complex activity controls metabolic and malignant phenotype in cancer cells J Biol Chem 283 2008 22700 22708
44. R.C. Sun, M. Fadia, J.E. Dahlstrom, C.R. Parish, P.G. Board, and A.C. Blackburn Reversal of the glycolytic phenotype by dichloroacetate inhibits metastatic breast cancer cell growth in vitro and in vivo Breast Cancer Res Treat 120 2010 253 260
45. E.D. Michelakis, G. Sutendra, P. Dromparis, L. Webster, A. Haromy, E. Niven, C. Maguire, T.L. Gammer, J.R. Mackey, D. Fulton, B. Abdulkarim, M.S. McMurtry, and K.C. Petruk Metabolic modulation of glioblastoma with dichloroacetate Sci Transl Med 2 2010 31ra34
46. J.W. Kim, I. Tchernyshyov, G.L. Semenza, and C.V. Dang HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia Cell Metab 3 2006 177 185
47. T. Contractor, and C.R. Harris p53 negatively regulates transcription of the pyruvate dehydrogenase kinase Pdk2 Cancer Res 72 2012 560 567
48. I. Magrath, Y.J. Lee, T. Anderson, W. Henle, J. Ziegler, R. Simon, and P. Schein Prognostic factors in Burkitt's lymphoma: importance of total tumor burden Cancer 45 1980 1507 1515
49. V.R. Fantin, J. St-Pierre, and P. Leder Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance Cancer Cell 9 2006 425 434
50. H. Shim, C. Dolde, B.C. Lewis, C.S. Wu, G. Dang, R.A. Jungmann, R. Dalla-Favera, and C.V. Dang c-Myc transactivation of LDH-A: implications for tumor metabolism and growth Proc Natl Acad Sci U S A 94 1997 6658 6663
51. C. Granchi, S. Roy, A. De Simone, I. Salvetti, T. Tuccinardi, A. Martinelli, M. Macchia, M. Lanza, L. Betti, G. Giannaccini, A. Lucacchini, E. Giovannetti, R. Sciarrillo, G.J. Peters, and F. Minutolo N-hydroxyindole-based inhibitors of lactate dehydrogenase against cancer cell proliferation Eur J Med Chem 46 2011 5398 5407
52. J. Hao, H. Chen, M.C. Madigan, P.J. Cozzi, J. Beretov, W. Xiao, W.J. Delprado, P.J. Russell, and Y. Li Co-expression of CD147 (EMMPRIN), CD44v3-10, MDR1 and monocarboxylate transporters is associated with prostate cancer drug resistance and progression Br J Cancer 103 2010 1008 1018
53. P. Sonveaux, F. Vegran, T. Schroeder, M.C. Wergin, J. Verrax, Z.N. Rabbani, C.J. De Saedeleer, K.M. Kennedy, C. Diepart, B.F. Jordan, M.J. Kelley, B. Gallez, M.L. Wahl, O. Feron, and M.W. Dewhirst Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice J Clin Invest 118 2008 3930 3942
54. R. Boidot, F. Vegran, A. Meulle, A. Le Breton, C. Dessy, P. Sonveaux, S. Lizard-Nacol, and O. Feron Regulation of monocarboxylate transporter MCT1 expression by p53 mediates inward and outward lactate fluxes in tumors Cancer Res 72 2012 939 948
55. Y. Wang, Y. Wang, L. Shen, Y. Pang, Z. Qiao, and P. Liu Prognostic and therapeutic implications of increased ATP citrate lyase expression in human epithelial ovarian cancer Oncol Rep 27 2012 1156 1162
56. G. Hatzivassiliou, F. Zhao, D.E. Bauer, C. Andreadis, A.N. Shaw, D. Dhanak, S.R. Hingorani, D.A. Tuveson, and C.B. Thompson ATP citrate lyase inhibition can suppress tumor cell growth Cancer Cell 8 2005 311 321
57. B.D. Manning, and L.C. Cantley AKT/PKB signaling: navigating downstream Cell 129 2007 1261 1274
58. M. Hassanein, M.D. Hoeksema, M. Shiota, J. Qian, B.K. Harris, H. Chen, J.E. Clark, W.E. Alborn, R. Eisenberg, and P.P. Massion SLC1A5 mediates glutamine transport required for lung cancer cell growth and survival Clin Cancer Res 19 2013 560 570
59. E.L. Carr, A. Kelman, G.S. Wu, R. Gopaul, E. Senkevitch, A. Aghvanyan, A.M. Turay, and K.A. Frauwirth Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation J Immunol 185 2010 1037 1044
60. 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 U S A 105 2008 18782 18787
61. 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
62. M.J. Seltzer, B.D. Bennett, A.D. Joshi, P. Gao, A.G. Thomas, D.V. Ferraris, T. Tsukamoto, C.J. Rojas, B.S. Slusher, J.D. Rabinowitz, C.V. Dang, and G.J. Riggins Inhibition of glutaminase preferentially slows growth of glioma cells with mutant IDH1 Cancer Res 70 2010 8981 8987
63. 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, M.D. Hogarty, and M.C. Simon ATF4 regulates MYC-mediated neuroblastoma cell death upon glutamine deprivation Cancer Cell 22 2012 631 644
64. 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
65. S. Rodriguez-Enriquez, P.A. Vital-Gonzalez, F.L. Flores-Rodriguez, A. Marin-Hernandez, L. Ruiz-Azuara, and R. Moreno-Sanchez Control of cellular proliferation by modulation of oxidative phosphorylation in human and rodent fast-growing tumor cells Toxicol Appl Pharmacol 215 2006 208 217
66. M. Guppy, P. Leedman, X. Zu, and V. Russell Contribution by different fuels and metabolic pathways to the total ATP turnover of proliferating MCF-7 breast cancer cells Biochem J 364 2002 309 315
67. R. Moreno-Sanchez, S. Rodriguez-Enriquez, E. Saavedra, A. Marin-Hernandez, and J.C. Gallardo-Perez The bioenergetics of cancer: is glycolysis the main ATP supplier in all tumor cells? Biofactors 35 2009 209 225
68. H.R. Christofk, M.G. Vander Heiden, N. Wu, J.M. Asara, and L.C. Cantley Pyruvate kinase M2 is a phosphotyrosine-binding protein Nature 452 2008 181 186
69. S. Mazurek, C.B. Boschek, F. Hugo, and E. Eigenbrodt Pyruvate kinase type M2 and its role in tumor growth and spreading Semin Cancer Biol 15 2005 300 308
70. B. Chaneton, P. Hillmann, L. Zheng, A.C. Martin, O.D. Maddocks, A. Chokkathukalam, J.E. Coyle, A. Jankevics, F.P. Holding, K.H. Vousden, C. Frezza, M. O'Reilly, and E. Gottlieb Serine is a natural ligand and allosteric activator of pyruvate kinase M2 Nature 491 2012 458 462
71. W. Luo, H. Hu, R. Chang, J. Zhong, M. Knabel, R. O'Meally, R.N. Cole, A. Pandey, and G.L. Semenza Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1 Cell 145 2011 732 744
72. M.I. Koukourakis, A. Giatromanolaki, E. Sivridis, G. Bougioukas, V. Didilis, K.C. Gatter, and A.L. Harris Lactate dehydrogenase-5 (LDH-5) overexpression in non-small-cell lung cancer tissues is linked to tumour hypoxia, angiogenic factor production and poor prognosis Br J Cancer 89 2003 877 885
73. H. Chen, L. Wang, J. Beretov, J. Hao, W. Xiao, and Y. Li Co-expression of CD147/EMMPRIN with monocarboxylate transporters and multiple drug resistance proteins is associated with epithelial ovarian cancer progression Clin Exp Metastasis 27 2010 557 569
74. C. Pinheiro, A. Longatto-Filho, K. Simoes, C.E. Jacob, C.J. Bresciani, B. Zilberstein, I. Cecconello, V.A. Alves, F. Schmitt, and F. Baltazar The prognostic value of CD147/EMMPRIN is associated with monocarboxylate transporter 1 co-expression in gastric cancer Eur J Cancer 45 2009 2418 2424
75. C. Pinheiro, A. Longatto-Filho, S.M. Pereira, D. Etlinger, M.A. Moreira, L.F. Jubé, G.S. Queiroz, F. Schmitt, and F. Baltazar Monocarboxylate transporters 1 and 4 are associated with CD147 in cervical carcinoma Dis Markers 26 2009 97 103
76. E. Giovannucci, D.M. Harlan, M.C. Archer, R.M. Bergenstal, S.M. Gapstur, L.A. Habel, M. Pollak, J.G. Regensteiner, and D. Yee Diabetes and cancer: a consensus report Diabetes Care 33 2010 1674 1685
77. M. Sanchez-Arago, M. Chamorro, and J.M. Cuezva Selection of cancer cells with repressed mitochondria triggers colon cancer progression Carcinogenesis 31 2010 567 576
78. G. Kroemer, and J. Pouyssegur Tumor cell metabolism: cancer's Achilles' heel Cancer Cell 13 2008 472 482
79. 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 U S A 104 2007 19345 19350
80. R.W. Moreadith, and A.L. Lehninger The pathways of glutamate and glutamine oxidation by tumor cell mitochondria: role of mitochondrial NAD(P)+-dependent malic enzyme J Biol Chem 259 1984 6215 6221
81. H. Simonnet, N. Alazard, K. Pfeiffer, C. Gallou, C. Beroud, J. Demont, R. Bouvier, H. Schagger, and C. Godinot Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma Carcinogenesis 23 2002 759 768
82. F. Lopez-Rios, M. Sanchez-Arago, E. Garcia-Garcia, A.D. Ortega, J.R. Berrendero, F. Pozo-Rodriguez, A. Lopez-Encuentra, C. Ballestin, and J.M. Cuezva Loss of the mitochondrial bioenergetic capacity underlies the glucose avidity of carcinomas Cancer Res 67 2007 9013 9017
83. A. Chatterjee, E. Mambo, and D. Sidransky Mitochondrial DNA mutations in human cancer Oncogene 25 2006 4663 4674
84. F. Sotgia, U.E. Martinez-Outschoorn, S. Pavlides, A. Howell, R.G. Pestell, and M.P. Lisanti Understanding the Warburg effect and the prognostic value of stromal caveolin-1 as a marker of a lethal tumor microenvironment Breast Cancer Res 13 2011 213
85. V. Fogal, A.D. Richardson, P.P. Karmali, I.E. Scheffler, J.W. Smith, and E. Ruoslahti Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation Mol Cell Biol 30 2010 1303 1318
86. M. Yu, Y. Shi, X. Wei, Y. Yang, Y. Zhou, X. Hao, N. Zhang, and R. Niu Depletion of mitochondrial DNA by ethidium bromide treatment inhibits the proliferation and tumorigenesis of T47D human breast cancer cells Toxicol Lett 170 2007 83 93
87. O. Catalina-Rodriguez, V.K. Kolukula, Y. Tomita, A. Preet, F. Palmieri, A. Wellstein, S. Byers, A.J. Giaccia, E. Glasgow, C. Albanese, and M.L. Avantaggiati The mitochondrial citrate transporter, CIC, is essential for mitochondrial homeostasis Oncotarget 3 2012 1220 1235
88. A. Orimo, P.B. Gupta, D.C. Sgroi, F. Arenzana-Seisdedos, T. Delaunay, R. Naeem, V.J. Carey, A.L. Richardson, and R.A. Weinberg Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion Cell 121 2005 335 348
89. A.E. Karnoub, A.B. Dash, A.P. Vo, A. Sullivan, M.W. Brooks, G.W. Bell, A.L. Richardson, K. Polyak, R. Tubo, and R.A. Weinberg Mesenchymal stem cells within tumour stroma promote breast cancer metastasis Nature 449 2007 557 563
90. D. Whitaker-Menezes, U.E. Martinez-Outschoorn, N. Flomenberg, R.C. Birbe, A.K. Witkiewicz, A. Howell, S. Pavlides, A. Tsirigos, A. Ertel, R.G. Pestell, P. Broda, C. Minetti, M.P. Lisanti, and F. Sotgia Hyperactivation of oxidative mitochondrial metabolism in epithelial cancer cells in situ: visualizing the therapeutic effects of metformin in tumor tissue Cell Cycle 10 2011 4047 4064
91. U.E. Martinez-Outschoorn, R.G. Pestell, A. Howell, M.L. Tykocinski, F. Nagajyothi, F.S. Machado, H.B. Tanowitz, F. Sotgia, and M.P. Lisanti Energy transfer in "parasitic" cancer metabolism: mitochondria are the powerhouse and Achilles' heel of tumor cells Cell Cycle 10 2011 4208 4216
92. U.E. Martinez-Outschoorn, S. Pavlides, A. Howell, R.G. Pestell, H.B. Tanowitz, F. Sotgia, and M.P. Lisanti Stromal-epithelial metabolic coupling in cancer: integrating autophagy and metabolism in the tumor microenvironment Int J Biochem Cell Biol 43 2011 1045 1051
93. U.E. Martinez-Outschoorn, R.M. Balliet, D.B. Rivadeneira, B. Chiavarina, S. Pavlides, C. Wang, D. Whitaker-Menezes, K.M. Daumer, Z. Lin, A.K. Witkiewicz, N. Flomenberg, A. Howell, R.G. Pestell, E.S. Knudsen, F. Sotgia, and M.P. Lisanti Oxidative stress in cancer associated fibroblasts drives tumor-stroma co-evolution: a new paradigm for understanding tumor metabolism, the field effect and genomic instability in cancer cells Cell Cycle 9 2010 3256 3276
94. 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
95. R.J. Shaw, and L.C. Cantley Ras, PI(3)K and mTOR signalling controls tumour cell growth Nature 441 2006 424 430
96. R.J. Deberardinis, J.J. Lum, and C.B. Thompson Phosphatidylinositol 3-kinase-dependent modulation of carnitine palmitoyltransferase 1A expression regulates lipid metabolism during hematopoietic cell growth J Biol Chem 281 2006 37372 37380
97. C.E. Nesbit, J.M. Tersak, and E.V. Prochownik MYC oncogenes and human neoplastic disease Oncogene 18 1999 3004 3016
98. D.M. Miller, S.D. Thomas, A. Islam, D. Muench, and K. Sedoris c-Myc and cancer metabolism Clin Cancer Res 18 2012 5546 5553
99. M. Yuneva, N. Zamboni, P. Oefner, R. Sachidanandam, and Y. Lazebnik Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells J Cell Biol 178 2007 93 105
100. W.G. Kaelin Jr., and P.J. Ratcliffe Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway Mol Cell 30 2008 393 402
101. G.L. Semenza Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics Oncogene 29 2010 625 634
102. K.H. Vousden, and C. Prives Blinded by the light: the growing complexity of p53 Cell 137 2009 413 431
103. T. Schmid, J. Zhou, R. Kohl, and B. Brune p300 relieves p53-evoked transcriptional repression of hypoxia-inducible factor-1 (HIF-1) Biochem J 380 2004 289 295
104. T. Li, N. Kon, L. Jiang, M. Tan, T. Ludwig, Y. Zhao, R. Baer, and W. Gu Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence Cell 149 2012 1269 1283
105. O.C. Rodriguez, S. Choudhury, V. Kolukula, E.E. Vietsch, J. Catania, A. Preet, K. Reynoso, J. Bargonetti, A. Wellstein, C. Albanese, and M.L. Avantaggiati Dietary downregulation of mutant p53 levels via glucose restriction: mechanisms and implications for tumor therapy Cell Cycle 11 2012 4436 4446
106. S.H. Moon, and C. Prives Mutant p53 succumbs to starvation Cell Cycle 12 2013 867
107. R. Brosh, and V. Rotter When mutants gain new powers: news from the mutant p53 field Nat Rev Cancer 9 2009 701 713
108. B.J. Altman, and C.V. Dang Normal and cancer cell metabolism: lymphocytes and lymphoma FEBS J 279 2012 2598 2609
109. 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
110. S. Christen, and U. Sauer Intracellular characterization of aerobic glucose metabolism in seven yeast species by 13C flux analysis and metabolomics FEMS Yeast Res 11 2011 263 272
111. T. Simsek, F. Kocabas, J. Zheng, R.J. Deberardinis, A.I. Mahmoud, E.N. Olson, J.W. Schneider, C.C. Zhang, and H.A. Sadek The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche Cell Stem Cell 7 2010 380 390
112. K. Takubo, G. Nagamatsu, C.I. Kobayashi, A. Nakamura-Ishizu, H. Kobayashi, E. Ikeda, N. Goda, Y. Rahimi, R.S. Johnson, T. Soga, A. Hirao, M. Suematsu, and T. Suda Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells Cell Stem Cell 12 2013 49 61
113. 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
114. C.H. Chang, J.D. Curtis, L.B. Maggi Jr., B. Faubert, A.V. Villarino, D. O'Sullivan, S.C. Huang, G.J. van der Windt, J. Blagih, J. Qiu, J.D. Weber, E.J. Pearce, R.G. Jones, and E.L. Pearce Posttranscriptional control of T cell effector function by aerobic glycolysis Cell 153 2013 1239 1251
115. E.A. Newsholme, B. Crabtree, and M.S. Ardawi The role of high rates of glycolysis and glutamine utilization in rapidly dividing cells Biosci Rep 5 1985 393 400
116. D. Molenaar, R. van Berlo, D. de Ridder, and B. Teusink Shifts in growth strategies reflect tradeoffs in cellular economics Mol Syst Biol 5 2009 323
117. A.L. Meadows, B. Kong, M. Berdichevsky, S. Roy, R. Rosiva, H.W. Blanch, and D.S. Clark Metabolic and morphological differences between rapidly proliferating cancerous and normal breast epithelial cells Biotechnol Prog 24 2008 334 341
118. P.L. Pedersen Warburg, me and hexokinase 2: multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the "Warburg Effect", i.e., elevated glycolysis in the presence of oxygen J Bioenerg Biomembr 39 2007 211 222
119. J.G. Pastorino, and J.B. Hoek Hexokinase II: the integration of energy metabolism and control of apoptosis Curr Med Chem 10 2003 1535 1551
120. H. Kimura, R.D. Braun, E.T. Ong, R. Hsu, T.W. Secomb, D. Papahadjopoulos, K. Hong, and M.W. Dewhirst Fluctuations in red cell flux in tumor microvessels can lead to transient hypoxia and reoxygenation in tumor parenchyma Cancer Res 56 1996 5522 5528
121. E.K. Rofstad, and T. Danielsen Hypoxia-induced metastasis of human melanoma cells: involvement of vascular endothelial growth factor-mediated angiogenesis Br J Cancer 80 1999 1697 1707
122. R. Martínez-Zaguilán, E.A. Seftor, R.E. Seftor, Y.W. Chu, R.J. Gillies, and M.J. Hendrix Acidic pH enhances the invasive behavior of human melanoma cells Clin Exp Metastasis 14 1996 176 186
123. O.K. Schlappack, A. Zimmermann, and R.P. Hill Glucose starvation and acidosis: effect on experimental metastatic potential: DNA content and MTX resistance of murine tumour cells Br J Cancer 64 1991 663 670
124. J. Rozhin, M. Sameni, G. Ziegler, and B.F. Sloane Pericellular pH affects distribution and secretion of cathepsin B in malignant cells Cancer Res 54 1994 6517 6525
125. Y.I. Rattigan, B.B. Patel, E. Ackerstaff, G. Sukenick, J.A. Koutcher, J.W. Glod, and D. Banerjee Lactate is a mediator of metabolic cooperation between stromal carcinoma associated fibroblasts and glycolytic tumor cells in the tumor microenvironment Exp Cell Res 318 2012 326 335
126. K. Fischer, P. Hoffmann, S. Voelkl, N. Meidenbauer, J. Ammer, M. Edinger, E. Gottfried, S. Schwarz, G. Rothe, S. Hoves, K. Renner, B. Timischl, A. Mackensen, L. Kunz-Schughart, R. Andreesen, S.W. Krause, and M. Kreutz Inhibitory effect of tumor cell-derived lactic acid on human T cells Blood 109 2007 3812 3819
127. S. Gottschalk, N. Anderson, C. Hainz, S.G. Eckhardt, and N.J. Serkova Imatinib (STI571)-mediated changes in glucose metabolism in human leukemia BCR-ABL-positive cells Clin Cancer Res 10 2004 6661 6668
128. H. Ying, A.C. Kimmelman, C.A. Lyssiotis, S. Hua, G.C. Chu, E. Fletcher-Sananikone, J.W. Locasale, J. Son, H. Zhang, J.L. Coloff, H. Yan, W. Wang, S. Chen, A. Viale, H. Zheng, J.H. Paik, C. Lim, A.R. Guimaraes, E.S. Martin, J. Chang, A.F. Hezel, S.R. Perry, J. Hu, B. Gan, Y. Xiao, J.M. Asara, R. Weissleder, Y.A. Wang, L. Chin, L.C. Cantley, and R.A. DePinho Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism Cell 149 2012 656 670
129. M.M. Reddy, M.S. Fernandes, A. Deshpande, E. Weisberg, H.V. Inguilizian, O. Abdel-Wahab, A.L. Kung, R.L. Levine, J.D. Griffin, and M. Sattler The JAK2V617F oncogene requires expression of inducible phosphofructokinase/ fructose-bisphosphatase 3 for cell growth and increased metabolic activity Leukemia 26 2012 481 489
130. T.N. Seyfried, and L.M. Shelton Cancer as a metabolic disease Nutr Metab 7 2010 7
131. S. Farber, and L.K. Diamond Temporary remissions in acute leukemia in children produced by folic acid antagonist, 4-aminopteroyl-glutamine acid N Engl J Med 238 1948 787 793