Metabolic plasticity as a determinant of tumor growth and metastasis

Cancer Research

Volumn 76, Issue 18, 2016, Pages 5201-5208

  Lehúede, Camille ^a,b   Dupuy, Fanny ^a,b   Rabinovitch, Rebecca ^a,b   Jones, Russell G ^a,b   Siegel, Peter M ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; AZD 3965; DICHLOROACETIC ACID; HYPOXIA INDUCIBLE FACTOR 1; METFORMIN; MONOCARBOXYLATE TRANSPORTER; PYRUVATE DEHYDROGENASE KINASE; PYRUVATE DEHYDROGENASE KINASE 1; UNCLASSIFIED DRUG;

ADVANCED CANCER; CANCER ASSOCIATED FIBROBLAST; CANCER CELL; CANCER STEM CELL; CARCINOGENESIS; CELL METABOLISM; CITRIC ACID CYCLE; DISTANT METASTASIS; ENERGY METABOLISM; EPITHELIAL MESENCHYMAL TRANSITION; GLYCOLYSIS; HUMAN; HYPOXIA; METABOLISM; METASTASIS; METASTATIC BREAST CANCER; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; REVERSE WARBURG EFFECT; REVIEW; SOLID TUMOR; STROMA; STROMA CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TUMOR INVASION;

ANIMALS; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84988955763     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0266     Document Type: Review

References (99)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
2. Yoshida GJ. Metabolic reprogramming: the emerging concept and associated therapeutic strategies. J Exp Clin Cancer Res 2015;34:111.
3. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 2011;27:441-64.
4. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer 2011;11:85-95.
5. Warburg O. On the origin of cancer cells. Science 1956;123:309-14.
6. Jose C, Bellance N, Rossignol R. Choosing between glycolysis and oxidative phosphorylation: a tumor's dilemma? Biochim Biophys Acta 2011;1807:552-61.
7. Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov 2011;10:671-84.
8. Ganapathy-Kanniappan S, Geschwind JF. Tumor glycolysis as a target for cancer therapy: progress and prospects. Mol Cancer 2013;12:152.
9. Li Z, Zhang H. Reprogramming of glucose, fatty acid and amino acid metabolism for cancer progression. Cell Mol Life Sci 2016;73:377-92.
10. Sottnik JL, Lori JC, Rose BJ, Thamm DH. Glycolysis inhibition by 2-deoxy-D-glucose reverts the metastatic phenotype in vitro and in vivo. Clin Exp Metastasis 2011;28:865-75.
11. Moreno-Sanchez R, Rodriguez-Enriquez S, Marin-Hernandez A, Saavedra E. Energy metabolism in tumor cells. FEBS J 2007;274:1393-418.
12. Nakajima EC, Van Houten B. Metabolic symbiosis in cancer: refocusing the Warburg lens. Mol Carcinog 2013;52:329-37.
13. Elia I, Schmieder R, Christen S, Fendt SM. Organ-specific cancer metabolism and its potential for therapy. Handb Exp Pharmacol 2016;233:321-53.
14. Guppy M, Leedman P, Zu X, Russell V. Contribution by different fuels and metabolic pathways to the total ATP turnover of proliferating MCF-7 breast cancer cells. Biochem J 2002;364:309-15.
15. Obre E, Rossignol R. Emerging concepts in bioenergetics and cancer research: metabolic flexibility, coupling, symbiosis, switch, oxidative tumors, metabolic remodeling, signaling and bioenergetic therapy. Int J Biochem Cell Biol 2015;59:167-81.
16. Martinez-Reyes I, Diebold LP, Kong H, Schieber M, Huang H, Hensley CT, et al. TCA cycle and mitochondrial membrane potential are necessary for diverse biological functions. Mol Cell 2016;61:199-209.
17. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008;13:472-82.
18. Weinberg SE, Chandel NS. Targeting mitochondria metabolism for cancer therapy. Nat Chem Biol 2015;11:9-15.
19. Pollak M. Potential applications for biguanides in oncology. J Clin Invest 2013;123:3693-700.
20. Pollak M. Overcoming drug development bottlenecks with repurposing: repurposing biguanides to target energy metabolism for cancer treatment. Nat Med 2014;20:591-3.
21. Camirand A, Zakikhani M, Young F, Pollak M. Inhibition of insulin-like growth factor-1 receptor signaling enhances growth-inhibitory and proapoptotic effects of gefitinib (Iressa) in human breast cancer cells. Breast Cancer Res 2005;7:R570-9.
22. Ben Sahra I, Laurent K, Loubat A, Giorgetti-Peraldi S, Colosetti P, Auberger P, et al. The antidiabetic drug metformin exerts an antitumoral effect in vitro and in vivo through a decrease of cyclin D1 level. Oncogene 2008;27:3576-86.
23. Buzzai M, Jones RG, Amaravadi RK, Lum JJ, DeBerardinis RJ, Zhao F, et al. Systemic treatment with the antidiabetic drug metformin selectively impairs p53-deficient tumor cell growth. Cancer Res 2007;67:6745-52.
24. Griss T, Vincent EE, Egnatchik R, Chen J, Ma EH, Faubert B, et al. Metformin antagonizes cancer cell proliferation by suppressing mitochondrial-dependent biosynthesis. PLoS Biol 2015;13:e1002309.
25. Andrzejewski S, Gravel SP, Pollak M, St-Pierre J. Metformin directly acts on mitochondria to alter cellular bioenergetics. Cancer Metab 2014;2:12.
26. Wheaton WW, Weinberg SE, Hamanaka RB, Soberanes S, Sullivan LB, Anso E, et al. Metformin inhibits mitochondrial complex I of cancer cells to reduce tumorigenesis. Elife 2014;3:e02242.
27. Birsoy K, Possemato R, Lorbeer FK, Bayraktar EC, Thiru P, Yucel B, et al. Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides. Nature 2014;508:108-12.
28. Ma R, Zhang W, Tang K, Zhang H, Zhang Y, Li D, et al. Switch of glycolysis to gluconeogenesis by dexamethasone for treatment of hepatocarcinoma. Nat Commun 2013;4:2508.
29. Amann T, Hellerbrand C. GLUT1 as a therapeutic target in hepatocellular carcinoma. Expert Opin Ther Targets 2009;13:1411-27.
30. Long J, Lang ZW, Wang HG, Wang TL, Wang BE, Liu SQ. Glutamine synthetase as an early marker for hepatocellular carcinoma based on proteomic analysis of resected small hepatocellular carcinomas. Hepatobiliary Pancreat Dis Int 2010;9:296-305.
31. Calvisi DF, Wang C, Ho C, Ladu S, Lee SA, Mattu S, et al. Increased lipogenesis, induced by AKT-mTORC1-RPS6 signaling, promotes development of human hepatocellular carcinoma. Gastroenterology 2011;140:1071-83.
32. Haber RS, Rathan A, Weiser KR, Pritsker A, Itzkowitz SH, Bodian C, et al. GLUT1 glucose transporter expression in colorectal carcinoma: a marker for poor prognosis. Cancer 1998;83:34-40.
33. Graziano F, Ruzzo A, Giacomini E, Ricciardi T, Aprile G, Loupakis F, et al. Glycolysis gene expression analysis and selective metabolic advantage in the clinical progression of colorectal cancer. Pharmacogenomics J 2016 Mar 1. [Epub ahead of print].
34. Cui R, Shi XY. Expression of pyruvate kinase M2 in human colorectal cancer and its prognostic value. Int J Clin Exp Pathol 2015;8:11393-9.
35. Notarnicola M, Messa C, Caruso MG. A significant role of lipogenic enzymes in colorectal cancer. Anticancer Res 2012;32:2585-90.
36. Huang F, Zhang Q, Ma H, Lv Q, Zhang T. Expression of glutaminase is upregulated in colorectal cancer and of clinical significance. Int J Clin Exp Pathol 2014;7:1093-100.
37. Hussien R, Brooks GA. Mitochondrial and plasma membrane lactate transporter and lactate dehydrogenase isoform expression in breast cancer cell lines. Physiol Genomics 2011;43:255-64.
38. Doyen J, Trastour C, Ettore F, Peyrottes I, Toussant N, Gal J, et al. Expression of the hypoxia-inducible monocarboxylate transporter MCT4 is increased in triple negative breast cancer and correlates independently with clinical outcome. Biochem Biophys Res Commun 2014;451:54-61.
39. Choi J, Kim do H, Jung WH, Koo JS. Metabolic interaction between cancer cells and stromal cells according to breast cancer molecular subtype. Breast Cancer Res 2013;15:R78.
40. Timmerman LA, Holton T, Yuneva M, Louie RJ, Padro M, Daemen A, et al. Glutamine sensitivity analysis identifies the xCT antiporter as a common triple-negative breast tumor therapeutic target. Cancer Cell 2013;24:450-65.
41. Cao MD, Lamichhane S, Lundgren S, Bofin A, Fjosne H, Giskeodegard GF, et al. Metabolic characterization of triple negative breast cancer. BMC Cancer 2014;14:941.
42. Kung HN, Marks JR, Chi JT. Glutamine synthetase is a genetic determinant of cell type-specific glutamine independence in breast epithelia. PLoS Genet 2011;7:e1002229.
43. Tchou J, Sonnad SS, Bergey MR, Basu S, Tomaszewski J, Alavi A, et al. Degree of tumor FDG uptake correlates with proliferation index in triple negative breast cancer. Mol Imaging Biol 2010;12:657-62.
44. Santidrian AF, Matsuno-Yagi A, Ritland M, Seo BB, LeBoeuf SE, Gay LJ, et al. Mitochondrial complex I activity and NAD+/NADH balance regulate breast cancer progression. J Clin Invest 2013;123:1068-81.
45. Dupuy F, Tabariès S, Andrzejewski S, Dong Z, Blagih J, Annis MG, et al. PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer. Cell Metab 2015;22:577-89.
46. Simoes RV, Serganova IS, Kruchevsky N, Leftin A, Shestov AA, Thaler HT, et al. Metabolic plasticity of metastatic breast cancer cells: adaptation to changes in the microenvironment. Neoplasia 2015;17:671-84.
47. Costello LC, Franklin RB, Feng P. Mitochondrial function, zinc, and intermediary metabolism relationships in normal prostate and prostate cancer. Mitochondrion 2005;5:143-53.
48. Ben Sahra I, Tanti JF, Bost F. The combination of metformin and 2-deoxyglucose inhibits autophagy and induces AMPK-dependent apoptosis in prostate cancer cells. Autophagy 2010;6:670-1.
49. Minamimoto R, Uemura H, Sano F, Terao H, Nagashima Y, Yamanaka S, et al. The potential of FDG-PET/CT for detecting prostate cancer in patients with an elevated serum PSA level. Ann Nucl Med 2011;25:21-7.
50. Pertega-Gomes N, Felisbino S, Massie CE, Vizcaino JR, Coelho R, Sandi C, et al. A glycolytic phenotype is associated with prostate cancer progression and aggressiveness: a role for monocarboxylate transporters as metabolic targets for therapy. J Pathol 2015;236:517-30.
51. Pertega-Gomes N, Vizcaino JR, Attig J, Jurmeister S, Lopes C, Baltazar F. A lactate shuttle system between tumour and stromal cells is associated with poor prognosis in prostate cancer. BMC Cancer 2014;14:352.
52. Schlaepfer IR, Rider L, Rodrigues LU, Gijon MA, Pac CT, Romero L, et al. Lipid catabolism via CPT1 as a therapeutic target for prostate cancer. Mol Cancer Ther 2014;13:2361-71.
53. Vavere AL, Kridel SJ, Wheeler FB, Lewis JS. 1-11C-acetate as a PET radiopharmaceutical for imaging fatty acid synthase expression in prostate cancer. J Nucl Med 2008;49:327-34.
54. Zadra G, Photopoulos C, Loda M. The fat side of prostate cancer. Biochim Biophys Acta 2013;1831:1518-32.
55. Sonveaux P, Vegran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 2008;118:3930-42.
56. Baenke F, Dubuis S, Brault C, Weigelt B, Dankworth B, Griffiths B, et al. Functional screening identifies MCT4 as a key regulator of breast cancer cell metabolism and survival. J Pathol 2015;237:152-65.
57. Hong CS, Graham NA, Gu W, Espindola Camacho C, Mah V, Maresh EL, et al. MCT1 modulates cancer cell pyruvate export and growth of tumors that co-express MCT1 and MCT4. Cell Rep 2016;14:1590-601.
58. Luo M, Wicha MS. Metabolic plasticity of cancer stem cells. Oncotarget 2015;6:35141-2.
59. Viale A, Pettazzoni P, Lyssiotis CA, Ying H, Sanchez N, Marchesini M, et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature 2014;514:628-32.
60. Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013;19:1423-37.
61. Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, et al. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle 2009;8:3984-4001.
62. Bonuccelli G, Tsirigos A, Whitaker-Menezes D, Pavlides S, Pestell RG, Chiavarina B, et al. Ketones and lactate "fuel" tumor growth and metastasis: evidence that epithelial cancer cells use oxidative mitochondrial metabolism. Cell Cycle 2010;9:3506-14.
63. Martinez-Outschoorn UE, Lisanti MP, Sotgia F. Catabolic cancer-associated fibroblasts transfer energy and biomass to anabolic cancer cells, fueling tumor growth. Semin Cancer Biol 2014;25:47-60.
64. Xing Y, Zhao S, Zhou BP, Mi J. Metabolic reprogramming of the tumour microenvironment. FEBS J 2015;282:3892-8.
65. De Milito A, Fais S. Tumor acidity, chemoresistance and proton pump inhibitors. Fut Oncol 2005;1:779-86.
66. Witkiewicz AK, Whitaker-Menezes D, Dasgupta A, Philp NJ, Lin Z, Gandara R, et al. Using the "reverse Warburg effect" to identify high-risk breast cancer patients: stromal MCT4 predicts poor clinical outcome in triple-negative breast cancers. Cell Cycle 2012;11:1108-17.
67. Sivridis E, Giatromanolaki A, Koukourakis MI. Proliferating fibroblasts at the invading tumour edge of colorectal adenocarcinomas are associated with endogenous markers of hypoxia, acidity, and oxidative stress. J Clin Pathol 2005;58:1033-8.
68. Nieman KM, Kenny HA, Penicka CV, Ladanyi A, Buell-Gutbrod R, Zillhardt MR, et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat Med 2011;17:1498-503.
69. Biswas SK. Metabolic reprogramming of immune cells in cancer progression. Immunity 2015;43:435-49.
70. Haschemi A, Kosma P, Gille L, Evans CR, Burant CF, Starkl P, et al. The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism. Cell Metab 2012;15:813-26.
71. Chang CH, Qiu J, O'Sullivan D, Buck MD, Noguchi T, Curtis JD, et al. Metabolic competition in the tumor microenvironment is a driver of cancer progression. Cell 2015;162:1229-41.
72. Ho PC, Bihuniak JD, Macintyre AN, Staron M, Liu X, Amezquita R, et al. Phosphoenolpyruvate is a metabolic checkpoint of anti-tumor T cell responses. Cell 2015;162:1217-28.
73. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011;331:1559-64.
74. Husemann Y, Geigl JB, Schubert F, Musiani P, Meyer M, Burghart E, et al. Systemic spread is an early step in breast cancer. Cancer Cell 2008;13:58-68.
75. Klein CA. Parallel progression of primary tumours and metastases. Nat Rev Cancer 2009;9:302-12.
76. McCreery MQ, Halliwill KD, Chin D, Delrosario R, Hirst G, Vuong P, et al. Evolution of metastasis revealed by mutational landscapes of chemically induced skin cancers. Nat Med 2015;21:1514-20.
77. Brastianos PK, Carter SL, Santagata S, Cahill DP, Taylor-Weiner A, Jones RT, et al. Genomic characterization of brain metastases reveals branched evolution and potential therapeutic targets. Cancer Discov 2015;5:1164-77.
78. Ye X, Weinberg RA. Epithelial-mesenchymal plasticity: a central regulator of cancer progression. Trends Cell Biol 2015;25:675-86.
79. Kondaveeti Y, Guttilla Reed IK, White BA. Epithelial-mesenchymal transition induces similar metabolic alterations in two independent breast cancer cell lines. Cancer Lett 2015;364:44-58.
80. Bhowmik SK, Ramirez-Pena E, Arnold JM, Putluri V, Sphyris N, Michailidis G, et al. EMT-induced metabolite signature identifies poor clinical outcome. Oncotarget 2015;6:42651-60.
81. LeBleu VS, O'Connell JT, Gonzalez Herrera KN, Wikman H, Pantel K, Haigis MC, et al. PGC-1alpha mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat Cell Biol 2014;16:992-1003, 1-15.
82. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006;127:397-408.
83. Piskounova E, Agathocleous M, Murphy MM, Hu Z, Huddlestun SE, Zhao Z, et al. Oxidative stress inhibits distant metastasis by human melanoma cells. Nature 2015;527:186-91.
84. Lu X, Bennet B, Mu E, Rabinowitz J, Kang Y. Metabolomic changes accompanying transformation and acquisition of metastatic potential in a syngeneic mouse mammary tumor model. J Biol Chem 2010;285:9317-21.
85. Porporato PE, Payen VL, Perez-Escuredo J, De Saedeleer CJ, Danhier P, Copetti T, et al. A mitochondrial switch promotes tumor metastasis. Cell Rep 2014;8:754-66.
86. Olson KA, Schell JC, Rutter J. Pyruvate and metabolic flexibility: illuminating a path toward selective cancer therapies. Trends Biochem Sci 2016;41:219-30.
87. Kamarajugadda S, Stemboroski L, Cai Q, Simpson NE, Nayak S, Tan M, et al. Glucose oxidation modulates anoikis and tumor metastasis. Mol Cell Biol 2012;32:1893-907.
88. Papandreou I, Goliasova T, Denko NC. Anticancer drugs that target metabolism: Is dichloroacetate the new paradigm? Int J Cancer 2011;128:1001-8.
89. Michelakis ED, Webster L, Mackey JR. Dichloroacetate (DCA) as a potential metabolic-targeting therapy for cancer. Br J Cancer 2008;99:989-94.
90. Lu J, Tan M, Cai Q. The Warburg effect in tumor progression: mitochondrial oxidative metabolism as an anti-metastasis mechanism. Cancer Lett 2015;356(2 Pt A):156-64.
91. Jeoung NH. Pyruvate dehydrogenase kinases: therapeutic targets for diabetes and cancers. Diabetes Metab J 2015;39:188-97.
92. Saunier E, Benelli C, Bortoli S. The pyruvate dehydrogenase complex in cancer: An old metabolic gatekeeper regulated by new pathways and pharmacological agents. Int J Cancer 2016;138:809-17.
93. Zhang SL, Hu X, Zhang W, Yao H, Tam KY. Development of pyruvate dehydrogenase kinase inhibitors in medicinal chemistry with particular emphasis as anticancer agents. Drug Discov Today 2015;20:1112-9.
94. Yuneva MO, Fan TW, Allen TD, Higashi RM, Ferraris DV, Tsukamoto T, et al. The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type. Cell Metab 2012;15:157-70.
95. Chen J, Lee HJ, Wu X, Huo L, Kim SJ, Xu L, et al. Gain of glucose-independent growth upon metastasis of breast cancer cells to the brain. Cancer Res 2015;75:554-65.
96. Mashimo T, Pichumani K, Vemireddy V, Hatanpaa KJ, Singh DK, Sirasanagandla S, et al. Acetate is a bioenergetic substrate for human glioblastoma and brain metastases. Cell 2014;159:1603-14.
97. Loo JM, Scherl A, Nguyen A, Man FY, Weinberg E, Zeng Z, et al. Extracellular metabolic energetics can promote cancer progression. Cell 2015;160:393-406.
98. Webber J, Yeung V, Clayton A. Extracellular vesicles as modulators of the cancer microenvironment. Semin Cell Dev Biol 2015;40:27-34.
99. Fong MY, Zhou W, Liu L, Alontaga AY, Chandra M, Ashby J, et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol 2015;17:183-94.