ROS homeostasis and metabolism: A critical liaison for cancer therapy

Experimental and Molecular Medicine

Volumn 48, Issue 11, 2016, Pages

  Kim, Jaehong ^a   Kim, Jongdoo ^a   Bae, Jong Sup ^b  

^a Gachon University College of Medicine   (South Korea)

^b Kyungpook National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

4 [BIS(2 CHLOROETHYL)OXIDOAMINO]PHENYLALANINE; AG 120; BAY 87 2243; CITRATE SYNTHASE; DEOXYGLUCOSE; DICHLOROACETIC ACID; ENASIDENIB; EZN 2968; FUMARATE HYDRATASE; ISOCITRATE DEHYDROGENASE; ISOSORBIDE; MALATE DEHYDROGENASE (DECARBOXYLATING); METFORMIN; PYRUVATE DEHYDROGENASE; QUARFLOXIN; REACTIVE OXYGEN METABOLITE; RO 7070179; TLN 232; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; GLUCOSE;

ARTICLE; BLOOD VESSEL; CANCER CELL; CANCER THERAPY; DRUG EFFICACY; GLUCOSE METABOLISM; HOMEOSTASIS; HUMAN; METABOLIC REGULATION; METABOLISM; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; OXIDATIVE STRESS; STROMA CELL; TUMOR MICROENVIRONMENT; ANIMAL; DRUG EFFECTS; MOLECULARLY TARGETED THERAPY; NEOPLASM; OXIDATION REDUCTION REACTION; PROCEDURES;

ANIMALS; ANTINEOPLASTIC AGENTS; GLUCOSE; HOMEOSTASIS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR TARGETED THERAPY; NEOPLASMS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TUMOR MICROENVIRONMENT;

EID: 84994608607     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2016.119     Document Type: Article

References (186)

1. Warburg O, Wind F, Negelein E. The metabolism of tumors in the body. J Gen Physiol 1927; 8: 519-530.
2. Lu J, Tan M, Cai Q. The Warburg effect in tumor progression: mitochondrial oxidative metabolism as an anti-metastasis mechanism. Cancer Lett 2015; 356: 156-164.
3. Coller HA. Is cancer a metabolic disease? Am J Pathol 2014; 184: 4-17.
4. Schnabel J. Targeting tumour metabolism. Nat Rev Drug Discov 2010; 9: 503-504.
5. Galluzzi L, Kepp O, Vander Heiden MG, Kroemer G. Metabolic targets for cancer therapy. Nat Rev Drug Discov 2013; 12: 829-846.
6. Jones NP, Schulze A. Targeting cancer metabolism-Aiming at a tumour's sweet-spot. Drug Discov Today 2012; 17: 232-241.
7. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012; 21: 297-308.
8. Schulze A, Harris AL. How cancer metabolism is tuned for proliferation and vulnerable to disruption. Nature 2012; 491: 364-373.
9. Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer 2011; 11: 325-337.
10. Wallace DC. Mitochondria and cancer. Nat Rev Cancer 2012; 12: 685-698.
11. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009; 8: 579-591.
12. Granja S, Pinheiro C, Reis RM, Martinho O, Baltazar F. Glucose addiction in cancer therapy: advances and drawbacks. Curr Drug Metab 2015; 16: 221-242.
13. Ganapathy-Kanniappan S, Geschwind JF. Tumor glycolysis as a target for cancer therapy: progress and prospects. Mol Cancer 2013; 12: 152.
14. Panieri E, Santoro MM. ROS homeostasis and metabolism: a dangerous liason in cancer cells. Cell Death Dis 2016; 7: e2253.
15. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417: 1-13.
16. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry 2005; 70: 200-214.
17. Costa A, Scholer-Dahirel A, Mechta-Grigoriou F. The role of reactive oxygen species and metabolism on cancer cells and their microenvironment. Semin Cancer Biol 2014; 25: 23-32.
18. Fiaschi T, Chiarugi P. Oxidative stress, tumor microenvironment, and metabolic reprogramming: a diabolic liaison. Int J Cell Biol 2012; 2012: 762825.
19. Tafani M, Sansone L, Limana F, Arcangeli T, De Santis E, Polese M et al. The interplay of reactive oxygen species, hypoxia, inflammation, and sirtuins in cancer initiation and progression. Oxid Med Cell Longev 2016; 2016: 3907147.
20. Hitchler MJ, Domann FE. Redox regulation of the epigenetic landscape in cancer: a role for metabolic reprogramming in remodeling the epigenome. Free Radical Biol Med 2012; 53: 2178-2187.
21. Sun C, Zhang H, Ma XF, Zhou X, Gan L, Liu YY et al. Isoliquiritigenin enhances radiosensitivity of HepG2 cells via disturbance of redox status. Cell Biol Biophys 2013; 65: 433-444.
22. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer 2011; 11: 85-95.
23. Watson J. Oxidants, antioxidants and the current incurability of metastatic cancers. Open Biol 2013; 3: 120144.
24. Jorgenson TC, Zhong W, Oberley TD. Redox imbalance and biochemical changes in cancer. Cancer Res 2013; 73: 6118-6123.
25. Chaiswing L, Zhong W, Oberley TD. Increasing discordant antioxidant protein levels and enzymatic activities contribute to increasing redox imbalance observed during human prostate cancer progression. Free Radical Biol Med 2014; 67: 342-352.
26. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12: 401-410.
27. Harper ME, Antoniou A, Villalobos-Menuey E, Russo A, Trauger R, Vendemelio M et al. Characterization of a novel metabolic strategy used by drug-resistant tumor cells. FASEB J 2002; 16: 1550-1557.
28. 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: 1498-1503.
29. Keenan MM, Chi JT. Alternative fuels for cancer cells. Cancer J 2015; 21: 49-55.
30. Hensley CT, Wasti AT, DeBerardinis RJ. Glutamine and cancer: cell biology, physiology, and clinical opportunities. J Clin Invest 2013; 123: 3678-3684.
31. Yalcin A, Clem BF, Imbert-Fernandez Y, Ozcan SC, Peker S, O'Neal J et al. 6-Phosphofructo-2-kinase (PFKFB3) promotes cell cycle progression and suppresses apoptosis via Cdk1-mediated phosphorylation of p27. Cell Death Dis 2014; 5: e1337.
32. Clem BF, O'Neal J, Tapolsky G, Clem AL, Imbert-Fernandez Y, Kerr DA 2nd et al. Targeting 6-phosphofructo-2-kinase (PFKFB3) as a therapeutic strategy against cancer. Mol Cancer Ther 2013; 12: 1461-1470.
33. Dong C, Yuan T, Wu Y, Wang Y, Fan TW, Miriyala S et al. Loss of FBP1 by Snail-mediated repression provides metabolic advantages in basal-like breast cancer. Cancer Cell 2013; 23: 316-331.
34. Lee SY, Jeon HM, Ju MK, Kim CH, Yoon G, Han SI et al. Wnt/Snail signaling regulates cytochrome C oxidase and glucose metabolism. Cancer Res 2012; 72: 3607-3617.
35. David CJ, Chen M, Assanah M, Canoll P, Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2010; 463: 364-368.
36. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008; 452: 230-233.
37. Anastasiou D, Yu Y, Israelsen WJ, Jiang JK, Boxer MB, Hong BS et al. Pyruvate kinase M2 activators promote tetramer formation and suppress tumorigenesis. Nat Chem Biol 2012; 8: 839-847.
38. Christofk HR, Vander Heiden MG, Wu N, Asara JM, Cantley LC. Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 2008; 452: 181-186.
39. Lv L, Li D, Zhao D, Lin R, Chu Y, Zhang H et al. Acetylation targets the M2 isoform of pyruvate kinase for degradation through chaperone-mediated autophagy and promotes tumor growth. Mol Cell 2011; 42: 719-730.
40. Anastasiou D, Poulogiannis G, Asara JM, Boxer MB, Jiang JK, Shen M et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 2011; 334: 1278-1283.
41. Kung C, Hixon J, Choe S, Marks K, Gross S, Murphy E et al. Small molecule activation of PKM2 in cancer cells induces serine auxotrophy. Chem Biol 2012; 19: 1187-1198.
42. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 2010; 18: 553-567.
43. Cohen AL, Holmen SL, Colman H. IDH1 and IDH2 mutations in gliomas. Curr Neurol Neurosci 2013; 13: 345.
44. Ichimura K, Pearson DM, Kocialkowski S, Backlund LM, Chan R, Jones DT et al. IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. NeuroOncology 2009; 11: 341-347.
45. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutaratedependent dioxygenases. Cancer Cell 2011; 19: 17-30.
46. Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 2012; 483: 479-483.
47. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006; 3: 177-185.
48. Kluza J, Corazao-Rozas P, Touil Y, Jendoubi M, Maire C, Guerreschi P et al. Inactivation of the HIF-1alpha/PDK3 signaling axis drives melanoma toward mitochondrial oxidative metabolism and potentiates the therapeutic activity of pro-oxidants. Cancer Res 2012; 72: 5035-5047.
49. Lu CW, Lin SC, Chen KF, Lai YY, Tsai SJ. Induction of pyruvate dehydrogenase kinase-3 by hypoxia-inducible factor-1 promotes metabolic switch and drug resistance. J Biol Chem 2008; 283: 28106-28114.
50. Zhao T, Zhu Y, Morinibu A, Kobayashi M, Shinomiya K, Itasaka S et al. HIF-1-mediated metabolic reprogramming reduces ROS levels and facilitates the metastatic colonization of cancers in lungs. Sci Rep 2014; 4: 3793.
51. Sonanez-Organis JG, Rodriguez-Armenta M, Leal-Rubio B, Peregrino-Uriarte AB, Gomez-Jimenez S, Yepiz-Plascencia G. Alternative splicing generates two lactate dehydrogenase subunits differentially expressed during hypoxia via HIF-1 in the shrimp Litopenaeus vannamei. Biochimie 2012; 94: 1250-1260.
52. Firth JD, Ebert BL, Ratcliffe PJ. Hypoxic regulation of lactate dehydrogenase A. Interaction between hypoxia-inducible factor 1 and cAMP response elements. J Biol Chem 1995; 270: 21021-21027.
53. Ullah MS, Davies AJ, Halestrap AP. The plasma membrane lactate transporter MCT4, but not MCT1, is up-regulated by hypoxia through a HIF-1alpha-dependent mechanism. J Biol Chem 2006; 281: 9030-9037.
54. Pelicano H, Lu W, Zhou Y, Zhang W, Chen Z, Hu Y et al. Mitochondrial dysfunction and reactive oxygen species imbalance promote breast cancer cell motility through a CXCL14-mediated mechanism. Cancer Res 2009; 69: 2375-2383.
55. Tello D, Balsa E, Acosta-Iborra B, Fuertes-Yebra E, Elorza A, Ordonez A et al. Induction of the mitochondrial NDUFA4L2 protein by HIF-1alpha decreases oxygen consumption by inhibiting complex I activity. Cell Metab 2011; 14: 768-779.
56. Bonello S, Zahringer C, BelAiba RS, Djordjevic T, Hess J, Michiels C et al. Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 2007; 27: 755-761.
57. Gorlach A, Diebold I, Schini-Kerth VB, Berchner-Pfannschmidt U, Roth U, Brandes RP et al. Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: Role of the p22(phox)-containing NADPH oxidase. Circ Res 2001; 89: 47-54.
58. Faubert B, Boily G, Izreig S, Griss T, Samborska B, Dong Z et al. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo. Cell Metab 2013; 17: 113-124.
59. Zhang C, Liu J, Liang Y, Wu R, Zhao Y, Hong X et al. Tumour-Associated mutant p53 drives the Warburg effect. Nat Commun 2013; 4: 2935.
60. Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O et al. p53 regulates mitochondrial respiration. Science 2006; 312: 1650-1653.
61. Schwartzenberg-Bar-Yoseph F, Armoni M, Karnieli E. The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression. Cancer Res 2004; 64: 2627-2633.
62. Contractor T, Harris CR. p53 negatively regulates transcription of the pyruvate dehydrogenase kinase Pdk2. Cancer Res 2012; 72: 560-567.
63. Jiang P, Du W, Wang X, Mancuso A, Gao X, Wu M et al. p53 regulates biosynthesis through direct inactivation of glucose-6-phosphate dehydrogenase. Nat Cell Biol 2011; 13: 310-316.
64. Polimeni M, Voena C, Kopecka J, Riganti C, Pescarmona G, Bosia A et al. Modulation of doxorubicin resistance by the glucose-6-phosphate dehydrogenase activity. Biochem J 2011; 439: 141-149.
65. Won KY, Lim SJ, Kim GY, Kim YW, Han SA, Song JY et al. Regulatory role of p53 in cancer metabolism via SCO2 and TIGAR in human breast cancer. Hum Pathol 2012; 43: 221-228.
66. Dang CV. The interplay between MYC and HIF in the Warburg effect. Ernst Schering Found Symp Proc 2007; 35-53.
67. Miao P, Sheng S, Sun X, Liu J, Huang G. Lactate dehydrogenase A in cancer: a promising target for diagnosis and therapy. IUBMB Life 2013; 65: 904-910.
68. Shen L, O'Shea JM, Kaadige MR, Cunha S, Wilde BR, Cohen AL et al. Metabolic reprogramming in triple-negative breast cancer through Myc suppression of TXNIP. Proc Natl Acad Sci USA 2015; 112: 5425-5430.
69. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011; 35: 871-882.
70. Peterson CW, Ayer DE. An extended Myc network contributes to glucose homeostasis in cancer and diabetes. Front Biosci (Landmark Ed) 2011; 16: 2206-2223.
71. Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov 2011; 10: 671-684.
72. Tennant DA, Duran RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 2010; 10: 267-277.
73. Sborov DW, Haverkos BM, Harris PJ. Investigational cancer drugs targeting cell metabolism in clinical development. Expert Opin Investig Drugs 2015; 24: 79-94.
74. Schwartz L, Buhler L, Icard P, Lincet H, Steyaert JM. Metabolic treatment of cancer: intermediate results of a prospective case series. Anticancer Res 2014; 34: 973-980.
75. Pelicano H, Martin DS, Xu RH, Huang P. Glycolysis inhibition for anticancer treatment. Oncogene 2006; 25: 4633-4646.
76. Pedersen PL. 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 2007; 39: 211-222.
77. Wang J, Wang J, Dai J, Jung Y, Wei CL, Wang Y et al. A glycolytic mechanism regulating an angiogenic switch in prostate cancer. Cancer Res 2007; 67: 149-159.
78. Zieker D, Konigsrainer I, Tritschler I, Loffler M, Beckert S, Traub F et al. Phosphoglycerate kinase 1 a promoting enzyme for peritoneal dissemination in gastric cancer. Int J Cancer 2010; 126: 1513-1520.
79. Vander Heiden MG, Locasale JW, Swanson KD, Sharfi H, Heffron GJ, Amador-Noguez D et al. Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 2010; 329: 1492-1499.
80. Zhang W, Zhang SL, Hu X, Tam KY. Targeting tumor metabolism for cancer treatment: is pyruvate dehydrogenase kinases (PDKs) a viable anticancer target? Int J Biol Sci 2015; 11: 1390-1400.
81. Bauer DE, Hatzivassiliou G, Zhao F, Andreadis C, Thompson CB. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 2005; 24: 6314-6322.
82. Chirala SS, Wakil SJ. Structure and function of animal fatty acid synthase. Lipids 2004; 39: 1045-1053.
83. Labar G, Wouters J, Lambert DM. A review on the monoacylglycerol lipase: at the interface between fat and endocannabinoid signalling. Curr Med Chem 2010; 17: 2588-2607.
84. Casals N, Zammit V, Herrero L, Fado R, Rodriguez-Rodriguez R, Serra D. Carnitine palmitoyltransferase 1C: From cognition to cancer. Prog Lipid Res 2016; 61: 134-148.
85. Langbein S, Zerilli M, Zur Hausen A, Staiger W, Rensch-Boschert K, Lukan N et al. Expression of transketolase TKTL1 predicts colon and urothelial cancer patient survival: Warburg effect reinterpreted. Brit J Cancer 2006; 94: 578-585.
86. Tarze A, Deniaud A, Le Bras M, Maillier E, Molle D, Larochette N et al. GAPDH, a novel regulator of the pro-Apoptotic mitochondrial membrane permeabilization. Oncogene 2007; 26: 2606-2620.
87. Le A, Cooper CR, Gouw AM, Dinavahi R, Maitra A, Deck LM et al. Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proc Natl Acad Sci USA 2010; 107: 2037-2042.
88. Liu Y, Cao Y, Zhang W, Bergmeier S, Qian Y, Akbar H et al. A smallmolecule inhibitor of glucose transporter 1 downregulates glycolysis, induces cell-cycle arrest, and inhibits cancer cell growth in vitro and in vivo. Mol Cancer Ther 2012; 11: 1672-1682.
89. Doherty JR, Cleveland JL. Targeting lactate metabolism for cancer therapeutics. J Clin Invest 2013; 123: 3685-3692.
90. Tan Z, Xie N, Banerjee S, Cui H, Fu M, Thannickal VJ et al. The monocarboxylate transporter 4 is required for glycolytic reprogramming and inflammatory response in macrophages. J Biol Chem 2015; 290: 46-55.
91. Pike LS, Smift AL, Croteau NJ, Ferrick DA, Wu M. Inhibition of fatty acid oxidation by etomoxir impairs NADPH production and increases reactive oxygen species resulting in ATP depletion and cell death in human glioblastoma cells. Biochim Biophys Acta 2011; 1807: 726-734.
92. Li J, Csibi A, Yang S, Hoffman GR, Li C, Zhang E et al. Synthetic lethality of combined glutaminase and Hsp90 inhibition in mTORC1-driven tumor cells. Proc Natl Acad Sci USA 2015; 112: E21-E29.
93. Sharma PK, Bhardwaj R, Dwarakanath BS, Varshney R. Metabolic oxidative stress induced by a combination of 2-DG and 6-AN enhances radiation damage selectively in malignant cells via non-coordinated expression of antioxidant enzymes. Cancer Lett 2010; 295: 154-166.
94. Izaki S, Goto H, Yokota S. Increased chemosensitivity and elevated reactive oxygen species are mediated by glutathione reduction in glutamine deprived neuroblastoma cells. J Cancer Res Clin Oncol 2008; 134: 761-768.
95. Montero AJ, Jassem J. Cellular redox pathways as a therapeutic target in the treatment of cancer. Drugs 2011; 71: 1385-1396.
96. Klawitter J, Kominsky DJ, Brown JL, Klawitter J, Christians U, Leibfritz D et al. Metabolic characteristics of imatinib resistance in chronic myeloid leukaemia cells. Br J Pharmacol 2009; 158: 588-600.
97. Kluza J, Jendoubi M, Ballot C, Dammak A, Jonneaux A, Idziorek T et al. Exploiting mitochondrial dysfunction for effective elimination of imatinibresistant leukemic cells. PLoS ONE 2011; 6: e21924.
98. Martinez Marignac VL, Smith S, Toban N, Bazile M, Aloyz R. Resistance to Dasatinib in primary chronic lymphocytic leukemia lymphocytes involves AMPK-mediated energetic re-programming. Oncotarget 2013; 4: 2550-2566.
99. Fumarola C, Caffarra C, La Monica S, Galetti M, Alfieri RR, Cavazzoni A et al. Effects of sorafenib on energy metabolism in breast cancer cells: role of AMPK-mTORC1 signaling. Breast Cancer Res Treat 2013; 141: 67-78.
100. Lu H, Li X, Luo Z, Liu J, Fan Z. Cetuximab reverses the Warburg effect by inhibiting HIF-1-regulated LDH-A. Mol Cancer Ther 2013; 12: 2187-2199.
101. Hartwich J, Orr WS, Ng CY, Spence Y, Morton C, Davidoff AM. HIF-1 alpha activation mediates resistance to anti-Angiogenic therapy in neuroblastoma xenografts. J Pediatr Surg 2013; 48: 39-46.
102. Wellen KE, Thompson CB. A two-way street: reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol 2012; 13: 270-276.
103. Locasale JW, Cantley LC. Metabolic flux and the regulation of mammalian cell growth. Cell Metab 2011; 14: 443-451.
104. 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.
105. Kim J, Bae JS. Tumor-Associated Macrophages and Neutrophils in Tumor Microenvironment. Mediat Inflamm 2016; 2016: 6058147.
106. Sotgia F, Martinez-Outschoorn UE, Lisanti MP. Cancer metabolism: new validated targets for drug discovery. Oncotarget 2013; 4: 1309-1316.
107. Martinez-Outschoorn U, Sotgia F, Lisanti MP. Tumor microenvironment and metabolic synergy in breast cancers: critical importance of mitochondrial fuels and function. Semin Oncol 2014; 41: 195-216.
108. Echigoya Y, Morita S, Itou T, Sakai T. Effects of extracellular lactate on production of reactive oxygen species by equine polymorphonuclear leukocytes in vitro. Am J Vet Res 2012; 73: 1290-1298.
109. Milovanova TN, Bhopale VM, Sorokina EM, Moore JS, Hunt TK, Hauer-Jensen M et al. Lactate stimulates vasculogenic stem cells via the thioredoxin system and engages an autocrine activation loop involving hypoxia-inducible factor 1. Mol Cell Biol 2008; 28: 6248-6261.
110. Tong L, Chuang CC, Wu S, Zuo L. Reactive oxygen species in redox cancer therapy. Cancer Lett 2015; 367: 18-25.
111. Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res 2010; 44: 479-496.
112. Michalek RD, Rathmell JC. The metabolic life and times of a T-cell. Immunol Rev 2010; 236: 190-202.
113. Altman BJ, Dang CV. Normal and cancer cell metabolism: lymphocytes and lymphoma. FEBS J 2012; 279: 2598-2609.
114. Pietras K, Ostman A. Hallmarks of cancer: interactions with the tumor stroma. Exp Cell Res 2010; 316: 1324-1331.
115. 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: 3930-3942.
116. Van Hee VF, Perez-Escuredo J, Cacace A, Copetti T, Sonveaux P. Lactate does not activate NF-kappaB in oxidative tumor cells. Front Pharmacol 2015; 6: 228.
117. 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.
118. Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria in cancer cells: what is so special about them? Trends Cell Biol 2008; 18: 165-173.
119. Ryu JH, Li SH, Park HS, Park JW, Lee B, Chun YS. Hypoxia-inducible factor alpha subunit stabilization by NEDD8 conjugation is reactive oxygen species-dependent. J BiolChem 2011; 286: 6963-6970.
120. Zhang W, Trachootham D, Liu J, Chen G, Pelicano H, Garcia-Prieto C et al. Stromal control of cystine metabolism promotes cancer cell survival in chronic lymphocytic leukaemia. Nat Cell Biol 2012; 14: 276-286.
121. Xu D, Rovira II, Finkel T. Oxidants painting the cysteine chapel: redox regulation of PTPs. Dev Cell 2002; 2: 251-252.
122. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 1995; 270: 296-299.
123. Hayman SR, Leung N, Grande JP, Garovic VD. VEGF inhibition, hypertension, and renal toxicity. Curr Oncol Rep 2012; 14: 285-294.
124. Inai T, Mancuso M, Hashizume H, Baffert F, Haskell A, Baluk P et al. Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol 2004; 165: 35-52.
125. Welti J, Loges S, Dimmeler S, Carmeliet P. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J Clin Invest 2013; 123: 3190-3200.
126. Kim J. Introduction to cerebral cavernous malformation: a brief review. BMB Rep 2016; 49: 255-262.
127. De Bock K, Georgiadou M, Schoors S, Kuchnio A, Wong BW, Cantelmo AR et al. Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 2013; 154: 651-663.
128. Goveia J, Stapor P, Carmeliet P. Principles of targeting endothelial cell metabolism to treat angiogenesis and endothelial cell dysfunction in disease. EMBO Mol Med 2014; 6: 1105-1120.
129. Dranka BP, Hill BG, Darley-Usmar VM. Mitochondrial reserve capacity in endothelial cells: The impact of nitric oxide and reactive oxygen species. Free Radic Biol Med 2010; 48: 905-914.
130. Koziel A, Jarmuszkiewicz W. Aerobic metabolism and reactive oxygen species in endothelial cells. Postepy Biochem 2013; 59: 386-394.
131. Del Bufalo D, Trisciuoglio D, Scarsella M, D'Amati G, Candiloro A, Iervolino A et al. Lonidamine causes inhibition of angiogenesis-related endothelial cell functions. Neoplasia 2004; 6: 513-522.
132. Schoors S, De Bock K, Cantelmo AR, Georgiadou M, Ghesquiere B, Cauwenberghs S et al. Partial and transient reduction of glycolysis by PFKFB3 blockade reduces pathological angiogenesis. Cell Metab 2014; 19: 37-48.
133. Sonveaux P, Copetti T, De Saedeleer CJ, Vegran F, Verrax J, Kennedy KM et al. Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis. PLoS ONE 2012; 7: e33418.
134. Vegran F, Boidot R, Michiels C, Sonveaux P, Feron O. Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kappaB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 2011; 71: 2550-2560.
135. Xu Y, An X, Guo X, Habtetsion TG, Wang Y, Xu X et al. Endothelial PFKFB3 plays a critical role in angiogenesis. Arterioscler Thromb Vasc Biol 2014; 34: 1231-1239.
136. El Sayed SM, Mahmoud AA, El Sawy SA, Abdelaal EA, Fouad AM, Yousif RS et al. Warburg effect increases steady-state ROS condition in cancer cells through decreasing their antioxidant capacities (anticancer effects of 3-bromopyruvate through antagonizing Warburg effect). Med Hypotheses 2013; 81: 866-870.
137. Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov 2013; 12: 931-947.
138. Sayin VI, Ibrahim MX, Larsson E, Nilsson JA, Lindahl P, Bergo MO. Antioxidants accelerate lung cancer progression in mice. Sci Transl Med 2014; 6: 221ra15.
139. Sabharwal SS, Schumacker PT. Mitochondrial ROS in cancer: initiators, amplifiers or an Achilles' heel? Nat Rev Cancer 2014; 14: 709-721.
140. Klein EA, Thompson IM Jr, Tangen CM, Crowley JJ, Lucia MS, Goodman PJ et al. Vitamin E and the risk of prostate cancer: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 2011; 306: 1549-1556.
141. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 2007; 6: 280-293.
142. Ristow M, Schmeisser S. Extending life span by increasing oxidative stress. Free Radic Biol Med 2011; 51: 327-336.
143. Ristow M, Zarse K. How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 2010; 45: 410-418.
144. Glasauer A, Chandel NS. Targeting antioxidants for cancer therapy. Biochem Pharmacol 2014; 92: 90-101.
145. Fulda S, Galluzzi L, Kroemer G. Targeting mitochondria for cancer therapy. Nat Rev Drug Discov 2010; 9: 447-464.
146. Song IS, Jeong JY, Jeong SH, Kim HK, Ko KS, Rhee BD et al. Mitochondria as therapeutic targets for cancer stem cells. World J Stem Cells 2015; 7: 418-427.
147. Shen YC, Ou DL, Hsu C, Lin KL, Chang CY, Lin CY et al. Activating oxidative phosphorylation by a pyruvate dehydrogenase kinase inhibitor overcomes sorafenib resistance of hepatocellular carcinoma. Br J Cancer 2013; 108: 72-81.
148. Ros S, Schulze A. Glycolysis back in the limelight: systemic targeting of HK2 blocks tumor growth. Cancer Discov 2013; 3: 1105-1107.
149. Fan J, Ye J, Kamphorst JJ, Shlomi T, Thompson CB, Rabinowitz JD. Quantitative flux analysis reveals folate-dependent NADPH production. Nature 2014; 510: 298-302.
150. Lewis CA, Parker SJ, Fiske BP, McCloskey D, Gui DY, Green CR et al. Tracing compartmentalized NADPH metabolism in the cytosol and mitochondria of mammalian cells. Mol Cell 2014; 55: 253-263.
151. De Milito A, Fais S. Tumor acidity, chemoresistance and proton pump inhibitors. Future Oncol 2005; 1: 779-786.
152. Backos DS, Franklin CC, Reigan P. The role of glutathione in brain tumor drug resistance. Biochem Pharmacol 2012; 83: 1005-1012.
153. DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, Frese K et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011; 475: 106-109.
154. Boivin B, Tonks NK. PTP1B: mediating ROS signaling to silence genes. Mol Cell Oncol 2015; 2: e975633.
155. Bak DW, Weerapana E. Cysteine-mediated redox signalling in the mitochondria. Mol Biosyst 2015; 11: 678-697.
156. Miki H, Funato Y. Regulation of intracellular signalling through cysteine oxidation by reactive oxygen species. J Biochem 2012; 151: 255-261.
157. Lizama-Manibusan B, McLaughlin B. Redox modification of proteins as essential mediators of CNS autophagy and mitophagy. FEBS Lett 2013; 587: 2291-2298.
158. Butterfield DA, Dalle-Donne I. Redox proteomics. Antioxid Redox Signal 2012; 17: 1487-1489.
159. Hitosugi T, Chen J. Post-translational modifications and the Warburg effect. Oncogene 2014; 33: 4279-4285.
160. Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010; 327: 1000-1004.
161. Zhao D, Li FL, Cheng ZL, Lei QY. Impact of acetylation on tumor metabolism. Mol Cell Oncol 2014; 1: e963452.
162. Obata T, Matthes A, Koszior S, Lehmann M, Araujo WL, Bock R et al. Alteration of mitochondrial protein complexes in relation to metabolic regulation under short-term oxidative stress in Arabidopsis seedlings. Phytochemistry 2011; 72: 1081-1091.
163. Yi W, Clark PM, Mason DE, Keenan MC, Hill C, Goddard WA 3rd et al. Phosphofructokinase 1 glycosylation regulates cell growth and metabolism. Science 2012; 337: 975-980.
164. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K et al. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem 1999; 274: 22699-22704.
165. Okoh VO, Felty Q, Parkash J, Poppiti R, Roy D. Reactive oxygen species via redox signaling to PI3K/AKT pathway contribute to the malignant growth of 4-hydroxy estradiol-transformed mammary epithelial cells. PLoS ONE 2013; 8: e54206.
166. Deprez J, Vertommen D, Alessi DR, Hue L, Rider MH. Phosphorylation and activation of heart 6-phosphofructo-2-kinase by protein kinase B and other protein kinases of the insulin signaling cascades. J Biol Chem1997; 272: 17269-17275.
167. Agbor TA, Cheong A, Comerford KM, Scholz CC, Bruning U, Clarke A et al. Small ubiquitin-related modifier (SUMO)-1 promotes glycolysis in hypoxia. J Biol Chem 2011; 286: 4718-4726.
168. Giorgino F, de Robertis O, Laviola L, Montrone C, Perrini S, McCowen KC et al. The sentrin-conjugating enzyme mUbc9 interacts with GLUT4 and GLUT1 glucose transporters and regulates transporter levels in skeletal muscle cells. Proc Natl Acad Sci USA 2000; 97: 1125-1130.
169. Lalioti VS, Vergarajauregui S, Pulido D, Sandoval IV. The insulin-sensitive glucose transporter, GLUT4, interacts physically with Daxx. Two proteins with capacity to bind Ubc9 and conjugated to SUMO1. J Biol Chem 2002; 277: 19783-19791.
170. Lushchak OV, Piroddi M, Galli F, Lushchak VI. Aconitase posttranslational modification as a key in linkage between Krebs cycle, iron homeostasis, redox signaling, and metabolism of reactive oxygen species. Redox Rep 2014; 19: 8-15.
171. Mailloux RJ, Jin X, Willmore WG. Redox regulation of mitochondrial function with emphasis on cysteine oxidation reactions. Redox Biol 2014; 2: 123-139.
172. Go YM, Chandler JD, Jones DP. The cysteine proteome. Free Radic Biol Med 2015; 84: 227-245.
173. Tonks NK. Redox redux: revisiting PTPs and the control of cell signaling. Cell 2005; 121: 667-670.
174. Yang M, Haase AD, Huang FK, Coulis G, Rivera KD, Dickinson BC et al. Dephosphorylation of tyrosine 393 in argonaute 2 by protein tyrosine phosphatase 1B regulates gene silencing in oncogenic RAS-induced senescence. Mol Cell 2014; 55: 782-790.
175. Frank GD, Mifune M, Inagami T, Ohba M, Sasaki T, Higashiyama S et al. Distinct mechanisms of receptor and nonreceptor tyrosine kinase activation by reactive oxygen species in vascular smooth muscle cells: role of metalloprotease and protein kinase C-delta. Mol Cell Biol 2003; 23: 1581-1589.
176. Mehdi MZ, Azar ZM, Srivastava AK. Role of receptor and nonreceptor protein tyrosine kinases in H2O2-induced PKB and ERK1/2 signaling. Cell Biochem Biophys 2007; 47: 1-10.
177. Nilsson MB, Zage PE, Zeng L, Xu L, Cascone T, Wu HK et al. Multiple receptor tyrosine kinases regulate HIF-1alpha and HIF-2alpha in normoxia and hypoxia in neuroblastoma: implications for antiangiogenic mechanisms of multikinase inhibitors. Oncogene 2010; 29: 2938-2949.
178. Chiarugi P. PTPs versus PTKs: the redox side of the coin. Free Radic Res 2005; 39: 353-364.
179. Ostman A, Frijhoff J, Sandin A, Bohmer FD. Regulation of protein tyrosine phosphatases by reversible oxidation. J Biochem 2011; 150: 345-356.
180. Patel MS, Korotchkina LG. Regulation of mammalian pyruvate dehydrogenase complex by phosphorylation: complexity of multiple phosphorylation sites and kinases. Exp Mol Med 2001; 33: 191-197.
181. Hitosugi T, Fan J, Chung TW, Lythgoe K, Wang X, Xie J et al. Tyrosine phosphorylation of mitochondrial pyruvate dehydrogenase kinase 1 is important for cancer metabolism. Mol Cell 2011; 44: 864-877.
182. Kemble DJ, Sun G. Direct and specific inactivation of protein tyrosine kinases in the Src and FGFR families by reversible cysteine oxidation. Proc Natl Acad USA 2009; 106: 5070-5075.
183. Fan J, Hitosugi T, Chung TW, Xie J, Ge Q, Gu TL et al. Tyrosine phosphorylation of lactate dehydrogenase A is important for NADH/NAD (+) redox homeostasis in cancer cells. Mol Cell Biol 2011; 31: 4938-4950.
184. Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, Lythgoe K et al. Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2009; 2: ra73.
185. DeBerardinis RJ, Chandel NS. Fundamentals of cancer metabolism. Sci Adv 2016; 2: e1600200.
186. 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: 157-170.