The role of mitochondrial electron transport in tumorigenesis and metastasis

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 4, 2014, Pages 1454-1463

  Tan, An S ^a   Baty, James W ^a   Berridge, Michael V ^a  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

Author keywords

Metabolic flexibility; Metastasis; Mitochondrial electron transport; Mitochondrial mutation; Mitochondrial respiration; Tumorigenesis

Indexed keywords

CITRIC ACID; CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ANCHORAGE INDEPENDENT GROWTH; BIOENERGY; CARCINOGENESIS; CITRIC ACID CYCLE; CYBRID; D LOOP; DNA STRUCTURE; ENERGY METABOLISM; GENE DELETION; GLYCOLYSIS; HUMAN; METABOLIC DISORDER; METASTASIS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL GENOME; MITOCHONDRIAL RESPIRATION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

METABOLIC FLEXIBILITY; METASTASIS; MITOCHONDRIAL ELECTRON TRANSPORT; MITOCHONDRIAL MUTATION; MITOCHONDRIAL RESPIRATION; TUMORIGENESIS;

ANIMALS; CARCINOGENESIS; ELECTRON TRANSPORT; HUMANS; MITOCHONDRIA; MUTATION; NEOPLASM METASTASIS; TUMOR MICROENVIRONMENT;

EID: 84895525043     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.10.016     Document Type: Review

References (138)

1. L.M. Ferreira Cancer metabolism: the Warburg effect today Exp. Mol. Pathol. 89 2010 372 380
2. W.H. Koppenol, P.L. Bounds, and C.V. Dang Otto Warburg's contributions to current concepts of cancer metabolism Nat. Rev. Cancer 11 2011 325 337
3. O. Warburg Uber den stoffwechsel der tumoren 1926 Berlin-Dahlem (Julius Springer) Berlin
4. O. Warburg On the origin of cancer cells Science 123 1956 309 314
5. T.N. Seyfried Cancer as a Metabolic Disease On the Origin, Management and Prevention of Cancer 2012 John Wiley & Sons, Inc Hobken, New Jersey
6. P.S. Ward, and C.B. Thompson Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate Cancer Cell 21 2012 297 308
7. M.V. Berridge, P.M. Herst, and A.S. Tan Metabolic flexibility and cell hierarchy in metastatic cancer Mitochondrion 10 2010 584 588
8. R.J. DeBerardinis, A. Mancuso, and E. Daikhin et al. 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
9. P.M. Herst, and M.V. Berridge Cell hierarchy, metabolic flexibity and systems approaches to cancer treatment Curr. Pharm. Biotechnol. 14 2013 289 299
10. K. Smolkova, L. Plecita-Hlavata, and N. Bellance et al. Waves of gene regulation suppress and then restore oxidative phosphorylation in cancer cells Int. J. Biochem. Cell Biol. 43 2011 950 968
11. V. Chen, and E. Shtivelman CC3/TIP30 regulates metabolic adaptation of tumor cells to glucose limitation Cell Cycle 9 2010 4941 4953
12. A. Schulze, and A.L. Harris How cancer metabolism is tuned for proliferation and vulnerable to disruption Nature 491 2012 364 373
13. 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
14. Z. Chen, L. Wang, and Q. Wang et al. Histone modifications and chromatin organization in prostate cancer Epigenomics 2 2010 551 560
15. J.S. Isaacs, Y.J. Jung, and D.R. Mole et al. HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability Cancer Cell 8 2005 143 153
16. J.R. Toro, M.L. Nickerson, and M.H. Wei et al. Mutations in the fumarate hydratase gene cause hereditary leiomyomatosis and renal cell cancer in families in North America Am. J. Hum. Genet. 73 2003 95 106
17. J.P. Bayley, H.P. Kunst, and A. Cascon et al. SDHAF2 mutations in familial and sporadic paraganglioma and phaeochromocytoma Lancet Oncol. 11 2010 366 372
18. E.R. Mardis, L. Ding, and D.J. Dooling et al. Recurring mutations found by sequencing an acute myeloid leukemia genome N. Engl. J. Med. 361 2009 1058 1066
19. D.W. Parsons, S. Jones, and X. Zhang et al. An integrated genomic analysis of human glioblastoma multiforme Science 321 2008 1807 1812
20. J.W. Locasale, A.R. Grassian, and T. Melman et al. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis Nat. Genet. 43 2011 869 874
21. R. Possemato, K.M. Marks, and Y.D. Shaul et al. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer Nature 476 2011 346 350
22. R.J. Shaw, and L.C. Cantley Decoding key nodes in the metabolism of cancer cells: sugar & spice and all things nice, F1000 Biol. Reprod. 4 2012 2
23. J. Kaplon, L. Zheng, and K. Meissl et al. A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence Nature 498 2013 109 112
24. S.P. Mathupala, Y.H. Ko, and P.L. Pedersen Hexokinase-2 bound to mitochondria: cancer's stygian link to the "Warburg Effect" and a pivotal target for effective therapy Semin. Cancer Biol. 19 2009 17 24
25. H.R. Christofk, M.G. Vander Heiden, and M.H. Harris et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth Nature 452 2008 230 233
26. D.Y. Gui, C.A. Lewis, and M.G. Vander Heiden Allosteric regulation of PKM2 allows cellular adaptation to different physiological states Sci. Signal. 6 2013 pe7
27. S. Mazurek Pyruvate kinase type M2: a key regulator of the metabolic budget system in tumor cells Int. J. Biochem. Cell Biol. 43 2011 969 980
28. B. Martinez-Pastor, and R. Mostoslavsky Sirtuins, metabolism, and cancer Front. Pharmacol. 3 2012 22
29. C. Sebastian, F.K. Satterstrom, and M.C. Haigis et al. From sirtuin biology to human diseases: an update J. Biol. Chem. 287 2012 42444 42452
30. J. Yuan, K. Minter-Dykhouse, and Z. Lou A c-Myc-SIRT1 feedback loop regulates cell growth and transformation J. Cell Biol. 185 2009 203 211
31. L. Zhong, A. D'Urso, and D. Toiber et al. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha Cell 140 2010 280 293
32. S.C. Dryden, F.A. Nahhas, and J.E. Nowak et al. Role for human SIRT2 NAD-dependent deacetylase activity in control of mitotic exit in the cell cycle Mol. Cell. Biol. 23 2003 3173 3185
33. S.M. Jeong, C. Xiao, and L.W. Finley et al. SIRT4 has tumor-suppressive activity and regulates the cellular metabolic response to DNA damage by inhibiting mitochondrial glutamine metabolism Cancer Cell 23 2013 450 463
34. M.F. Barber, E. Michishita-Kioi, and Y. Xi et al. SIRT7 links H3K18 deacetylation to maintenance of oncogenic transformation Nature 487 2012 114 118
35. C.V. Dang, J.W. Kim, and P. Gao et al. The interplay between MYC and HIF in cancer Nat. Rev. Cancer 8 2008 51 56
36. A. Carracedo, L.C. Cantley, and P.P. Pandolfi Cancer metabolism: fatty acid oxidation in the limelight Nat. Rev. Cancer 13 2013 227 232
37. P.A. Gameiro, J. Yang, and A.M. Metelo et al. In vivo HIF-mediated reductive carboxylation is regulated by citrate levels and sensitizes VHL-deficient cells to glutamine deprivation Cell Metab. 17 2013 372 385
38. J. Son, C.A. Lyssiotis, and H. Ying et al. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway Nature 496 2013 101 105
39. D.R. Wise, and C.B. Thompson Glutamine addiction: a new therapeutic target in cancer Trends Biochem. Sci. 35 2010 427 433
40. D.C. Wallace Mitochondria and cancer Nat. Rev. Cancer 12 2012 685 698
41. A. Ertel, A. Tsirigos, and D. Whitaker-Menezes et al. Is cancer a metabolic rebellion against host aging? In the quest for immortality, tumor cells try to save themselves by boosting mitochondrial metabolism Cell Cycle 11 2012 253 263
42. R. Haq, J. Shoag, and P. Andreu-Perez et al. Oncogenic BRAF regulates oxidative metabolism via PGC1alpha and MITF Cancer Cell 23 2013 302 315
43. R. Moreno-Sanchez, S. Rodriguez-Enriquez, and A. Marin-Hernandez et al. Energy metabolism in tumor cells FEBS J. 274 2007 1393 1418
44. F. Vazquez, J.H. Lim, and H. Chim et al. PGC1alpha expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress Cancer Cell 23 2013 287 301
45. X.L. Zu, and M. Guppy Cancer metabolism: facts, fantasy, and fiction Biochem. Biophys. Res. Commun. 313 2004 459 465
46. L.I. Cardenas-Navia, D. Mace, and R.A. Richardson et al. The pervasive presence of fluctuating oxygenation in tumors Cancer Res. 68 2008 5812 5819
47. P. Jezek, L. Plecita-Hlavata, and K. Smolkova et al. Distinctions and similarities of cell bioenergetics and the role of mitochondria in hypoxia, cancer, and embryonic development Int. J. Biochem. Cell Biol. 42 2010 604 622
48. F. Hirschhaeuser, U.G. Sattler, and W. Mueller-Klieser Lactate: a metabolic key player in cancer Cancer Res. 71 2011 6921 6925
49. P.C. Nowell The clonal evolution of tumor cell populations Science 194 1976 23 28
50. D.J. Burgess Genomic instability: close-up on cancer copy number alterations Nat. Rev. Genet. 13 2012 5
51. M. Greaves, and C.C. Maley Clonal evolution in cancer Nature 481 2012 306 313
52. T. Kuukasjarvi, R. Karhu, and M. Tanner et al. Genetic heterogeneity and clonal evolution underlying development of asynchronous metastasis in human breast cancer Cancer Res. 57 1997 1597 1604
53. M.O. Yuneva, T.W. Fan, and T.D. Allen et al. The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type Cell Metab. 15 2012 157 170
54. G. Bonuccelli, D. Whitaker-Menezes, and R. Castello-Cros et al. The reverse Warburg effect: glycolysis inhibitors prevent the tumor promoting effects of caveolin-1 deficient cancer associated fibroblasts Cell Cycle 9 2010 1960 1971
55. R. Castello-Cros, G. Bonuccelli, and A. Molchansky et al. Matrix remodeling stimulates stromal autophagy, "fueling" cancer cell mitochondrial metabolism and metastasis Cell Cycle 10 2011 2021 2034
56. U.E. Martinez-Outschoorn, S. Pavlides, and A. Howell et al. Stromal-epithelial metabolic coupling in cancer: integrating autophagy and metabolism in the tumor microenvironment Int. J. Biochem. Cell Biol. 43 2011 1045 1051
57. S. Pavlides, A. Tsirigos, and I. Vera et al. Loss of stromal caveolin-1 leads to oxidative stress, mimics hypoxia and drives inflammation in the tumor microenvironment, conferring the "reverse Warburg effect": a transcriptional informatics analysis with validation Cell Cycle 9 2010 2201 2219
58. S. Pavlides, A. Tsirigos, and I. Vera et al. Transcriptional evidence for the "Reverse Warburg Effect" in human breast cancer tumor stroma and metastasis: similarities with oxidative stress, inflammation, Alzheimer's disease, and "Neuron-Glia Metabolic Coupling" Aging (Albany NY) 2 2010 185 199
59. S. Pavlides, D. Whitaker-Menezes, and R. Castello-Cros et al. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma Cell Cycle 8 2009 3984 4001
60. F. Sotgia, D. Whitaker-Menezes, and U.E. Martinez-Outschoorn et al. Mitochondria "fuel" breast cancer metabolism: fifteen markers of mitochondrial biogenesis label epithelial cancer cells, but are excluded from adjacent stromal cells Cell Cycle 11 2012 4390 4401
61. E.A. Schon, S. DiMauro, and M. Hirano Human mitochondrial DNA: roles of inherited and somatic mutations Nat. Rev. Genet. 13 2012 878 890
62. T.C. Larman, S.R. DePalma, and A.G. Hadjipanayis et al. Spectrum of somatic mitochondrial mutations in five cancers Proc. Natl. Acad. Sci. U. S. A. 109 2012 14087 14091
63. K. Polyak, Y. Li, and H. Zhu et al. Somatic mutations of the mitochondrial genome in human colorectal tumours Nat. Genet. 20 1998 291 293
64. L. Iommarini, M.A. Calvaruso, and I. Kurelac et al. Complex I impairment in mitochondrial diseases and cancer: parallel roads leading to different outcomes Int. J. Biochem. Cell Biol. 45 2013 47 63
65. J. Lu, L.K. Sharma, and Y. Bai Implications of mitochondrial DNA mutations and mitochondrial dysfunction in tumorigenesis Cell Res. 19 2009 802 815
66. H. Schagger, and K. Pfeiffer Supercomplexes in the respiratory chains of yeast and mammalian mitochondria EMBO J. 19 2000 1777 1783
67. D.R. Winge Sealing the mitochondrial respirasome Mol. Cell. Biol. 32 2012 2647 2652
68. R. Baradaran, J.M. Berrisford, and G.S. Minhas et al. Crystal structure of the entire respiratory complex I Nature 494 2013 443 448
69. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
70. S. Dasgupta, E. Soudry, and N. Mukhopadhyay et al. Mitochondrial DNA mutations in respiratory complex-I in never-smoker lung cancer patients contribute to lung cancer progression and associated with EGFR gene mutation J. Cell. Physiol. 227 2012 2451 2460
71. L.K. Sharma, H. Fang, and J. Liu et al. Mitochondrial respiratory complex I dysfunction promotes tumorigenesis through ROS alteration and AKT activation Hum. Mol. Genet. 20 2011 4605 4616
72. W. Sun, S. Zhou, and S.S. Chang et al. Mitochondrial mutations contribute to HIF1alpha accumulation via increased reactive oxygen species and up-regulated pyruvate dehydrogenease kinase 2 in head and neck squamous cell carcinoma Clin. Cancer Res. 15 2009 476 484
73. G. Gasparre, I. Kurelac, and M. Capristo et al. A mutation threshold distinguishes the antitumorigenic effects of the mitochondrial gene MTND1, an oncojanus function Cancer Res. 71 2011 6220 6229
74. J.S. Park, L.K. Sharma, and H. Li et al. A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis Hum. Mol. Genet. 18 2009 1578 1589
75. D. Astuti, F. Latif, and A. Dallol et al. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma Am. J. Hum. Genet. 69 2001 49 54
76. B.E. Baysal, R.E. Ferrell, and J.E. Willett-Brozick et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma Science 287 2000 848 851
77. M. Brandon, P. Baldi, and D.C. Wallace Mitochondrial mutations in cancer Oncogene 25 2006 4647 4662
78. S. Niemann, and U. Muller Mutations in SDHC cause autosomal dominant paraganglioma, type 3 Nat. Genet. 26 2000 268 270
79. S. Vanharanta, M. Buchta, and S.R. McWhinney et al. Early-onset renal cell carcinoma as a novel extraparaganglial component of SDHB-associated heritable paraganglioma Am. J. Hum. Genet. 74 2004 153 159
80. T. Bourgeron, P. Rustin, and D. Chretien et al. Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency Nat. Genet. 11 1995 144 149
81. J. Permuth-Wey, Y.A. Chen, and Y.Y. Tsai et al. Inherited variants in mitochondrial biogenesis genes may influence epithelial ovarian cancer risk Cancer Epidemiol. Biomarkers Prev. 20 2011 1131 1145
82. J.A. Petros, A.K. Baumann, and E. Ruiz-Pesini et al. mtDNA mutations increase tumorigenicity in prostate cancer Proc. Natl. Acad. Sci. U. S. A. 102 2005 719 724
83. R. Lehtonen, M. Kiuru, and S. Vanharanta et al. Biallelic inactivation of fumarate hydratase (FH) occurs in nonsyndromic uterine leiomyomas but is rare in other tumors Am. J. Pathol. 164 2004 17 22
84. L. Dang, D.W. White, and S. Gross et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate Nature 462 2009 739 744
85. R.J. DeBerardinis, and C.B. Thompson Cellular metabolism and disease: what do metabolic outliers teach us? Cell 148 2012 1132 1144
86. I.A. Barbosa, N.G. Machado, and A.J. Skildum et al. Mitochondrial remodeling in cancer metabolism and survival: potential for new therapies Biochim. Biophys. Acta 1826 2012 238 254
87. N.G. Ericson, M. Kulawiec, and M. Vermulst et al. Decreased mitochondrial DNA mutagenesis in human colorectal cancer PLoS Genet. 8 2012 e1002689
88. K. Skonieczna, B.A. Malyarchuk, and T. Grzybowski The landscape of mitochondrial DNA variation in human colorectal cancer on the background of phylogenetic knowledge Biochim. Biophys. Acta 1825 2012 153 159
89. R.W. Taylor, and D.M. Turnbull Mitochondrial DNA mutations in human disease Nat. Rev. Genet. 6 2005 389 402
90. M. Yu, Y. Shi, and X. Wei et al. Mitochondrial DNA depletion promotes impaired oxidative status and adaptive resistance to apoptosis in T47D breast cancer cells Eur. J. Cancer Prev. 18 2009 445 457
91. S.K. Mithani, I.M. Smith, and S.L. Topalian et al. Nonsynonymous somatic mitochondrial mutations occur in the majority of cutaneous melanomas Melanoma Res. 18 2008 214 219
92. Y. Guo, Q. Cai, and D.C. Samuels et al. The use of next generation sequencing technology to study the effect of radiation therapy on mitochondrial DNA mutation Mutat. Res. 744 2012 154 160
93. A.N. Howell, and R. Sager Tumorigenicity and its suppression in cybrids of mouse and Chinese hamster cell lines Proc. Natl. Acad. Sci. U. S. A. 75 1978 2358 2362
94. B.A. Israel, and W.I. Schaeffer Cytoplasmic suppression of malignancy In Vitro Cell. Dev. Biol. 23 1987 627 632
95. M. Koura, H. Isaka, and M.C. Yoshida et al. Suppression of tumorigenicity in interspecific reconstituted cells and cybrids Gann 73 1982 574 580
96. J.W. Shay, Y.N. Liu, and H. Werbin Cytoplasmic suppression of tumor progression in reconstituted cells Somat. Cell Mol. Genet. 14 1988 345 350
97. J.W. Shay, and H. Werbin Cytoplasmic suppression of tumorigenicity in reconstructed mouse cells Cancer Res. 48 1988 830 833
98. J. Hayashi, M. Takemitsu, and I. Nonaka Recovery of the missing tumorigenicity in mitochondrial DNA-less HeLa cells by introduction of mitochondrial DNA from normal human cells Somat. Cell Mol. Genet. 18 1992 123 129
99. J. Hayashi, H. Werbin, and J.W. Shay Effects of normal human fibroblast mitochondrial DNA on segregation of HeLaTG Mitochondrial DNA and on tumorigenicity of HeLaTG cells Cancer Res. 46 1986 4001 4006
100. M. Akimoto, M. Niikura, and M. Ichikawa et al. Nuclear DNA but not mtDNA controls tumor phenotypes in mouse cells Biochem. Biophys. Res. Commun. 327 2005 1028 1035
101. O. Hashizume, A. Shimizu, and M. Yokota et al. Specific mitochondrial DNA mutation in mice regulates diabetes and lymphoma development Proc. Natl. Acad. Sci. U. S. A. 109 2012 10528 10533
102. K. Ishikawa, K. Takenaga, and M. Akimoto et al. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis Science 320 2008 661 664
103. K. Ishikawa, O. Hashizume, and N. Koshikawa et al. Enhanced glycolysis induced by mtDNA mutations does not regulate metastasis FEBS Lett. 582 2008 3525 3530
104. A.F. Santidrian, A. Matsuno-Yagi, and M. Ritland et al. Mitochondrial complex I activity and NAD +/NADH balance regulate breast cancer progression J. Clin. Invest. 123 2013 1068 1081
105. R. Morais, K. Zinkewich-Peotti, and M. Parent et al. Tumor-forming ability in athymic nude mice of human cell lines devoid of mitochondrial DNA Cancer Res. 54 1994 3889 3896
106. L.R. Cavalli, M. Varella-Garcia, and B.C. Liang Diminished tumorigenic phenotype after depletion of mitochondrial DNA Cell Growth Differ. 8 1997 1189 1198
107. D. Magda, P. Lecane, and J. Prescott et al. mtDNA depletion confers specific gene expression profiles in human cells grown in culture and in xenograft BMC Genomics 9 2008 521
108. M. Kulawiec, A. Safina, and M.M. Desouki et al. Tumorigenic transformation of human breast epithelial cells induced by mitochondrial DNA depletion Cancer Biol. Ther. 7 2008 1732 1743
109. F. Weinberg, R. Hamanaka, and W.W. Wheaton et al. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity Proc. Natl. Acad. Sci. U. S. A. 107 2010 8788 8793
110. M.V. Berridge, and A.S. Tan Effects of mitochondrial gene deletion on tumorigenicity of metastatic melanoma: reassessing the Warburg effect Rejuvenation Res. 13 2010 139 141
111. C.A. Rebbeck, A.M. Leroi, and A. Burt Mitochondrial capture by a transmissible cancer Science 331 2011 303
112. Y.M. Cho, J.H. Kim, and M. Kim et al. Mesenchymal stem cells transfer mitochondria to the cells with virtually no mitochondrial function but not with pathogenic mtDNA mutations PLoS One 7 2012 e32778
113. H.H. Gerdes, and R.N. Carvalho Intercellular transfer mediated by tunneling nanotubes Curr. Opin. Cell Biol. 20 2008 470 475
114. J.L. Spees, S.D. Olson, and M.J. Whitney et al. Mitochondrial transfer between cells can rescue aerobic respiration Proc. Natl. Acad. Sci. U. S. A. 103 2006 1283 1288
115. B. Onfelt, S. Nedvetzki, and R.K. Benninger et al. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria J. Immunol. 177 2006 8476 8483
116. S. Weinhouse On respiratory impairment in cancer cells Science 124 1956 267 269
117. N.C. Denko Hypoxia, HIF1 and glucose metabolism in the solid tumour Nat. Rev. Cancer 8 2008 705 713
118. J.M. Funes, M. Quintero, and S. Henderson et al. Transformation of human mesenchymal stem cells increases their dependency on oxidative phosphorylation for energy production Proc. Natl. Acad. Sci. U. S. A. 104 2007 6223 6228
119. S. Mori, J.T. Chang, and E.R. Andrechek et al. Anchorage-independent cell growth signature identifies tumors with metastatic potential Oncogene 28 2009 2796 2805
120. S.M. Frisch, and H. Francis Disruption of epithelial cell-matrix interactions induces apoptosis J. Cell Biol. 124 1994 619 626
121. E. Giannoni, F. Buricchi, and G. Grimaldi et al. Redox regulation of anoikis: reactive oxygen species as essential mediators of cell survival Cell Death Differ. 15 2008 867 878
122. J. Rehman Empowering self-renewal and differentiation: the role of mitochondria in stem cells J. Mol. Med. (Berl.) 88 2010 981 986
123. E.H. Sarsour, M.G. Kumar, and L. Chaudhuri et al. Redox control of the cell cycle in health and disease Antioxid. Redox Signal. 11 2009 2985 3011
124. G. Gloire, S. Legrand-Poels, and J. Piette NF-kappaB activation by reactive oxygen species: fifteen years later Biochem. Pharmacol. 72 2006 1493 1505
125. Y.S. Bae, H. Oh, and S.G. Rhee et al. Regulation of reactive oxygen species generation in cell signaling Mol. Cell 32 2011 491 509
126. C.L. Quinlan, A.L. Orr, and I.V. Perevoshchikova et al. Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions J. Biol. Chem. 287 2012 27255 27264
127. D.C. Wallace A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine Annu. Rev. Genet. 39 2005 359 407
128. M. Schauen, D. Spitkovsky, and J. Schubert et al. Respiratory chain deficiency slows down cell-cycle progression via reduced ROS generation and is associated with a reduction of p21CIP1/WAF1 J. Cell. Physiol. 209 2006 103 112
129. K. Zinkewich-Peotti, M. Parent, and R. Morais Mitochondrial DNA modulation of the anchorage-independent phenotype of transformed avian cells Cancer Res. 50 1990 6675 6682
130. K. Zinkewich-Peotti, M. Parent, and R. Morais On the tumorigenicity of mitochondrial DNA-depleted avian cells Cancer Lett. 59 1991 119 124
131. J.A. Hickman Apoptosis and chemotherapy resistance Eur. J. Cancer 32A 1996 921 926
132. M.A. Nikiforov, K. Hagen, and V.S. Ossovskaya et al. p53 modulation of anchorage independent growth and experimental metastasis Oncogene 13 1996 1709 1719
133. S.A. Susin, N. Zamzami, and M. Castedo et al. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease J. Exp. Med. 184 1996 1331 1341
134. C.A. Kruse, D.H. Mitchell, and B.K. Kleinschmidt-DeMasters et al. Characterization of a continuous human glioma cell line DBTRG-05MG: growth kinetics, karyotype, receptor expression, and tumor suppressor gene analyses In Vitro Cell. Dev. Biol. 28A 1992 609 614
135. Z. Liu, and R.A. Butow A transcriptional switch in the expression of yeast tricarboxylic acid cycle genes in response to a reduction or loss of respiratory function Mol. Cell. Biol. 19 1999 6720 6728
136. L.J. Reitzer, B.M. Wice, and D. Kennell Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells J. Biol. Chem. 254 1979 2669 2676
137. A.R. Mullen, W.W. Wheaton, and E.S. Jin et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria Nature 481 2012 385 388
138. Y.N. Kim, K.H. Koo, and J.Y. Sung et al. Anoikis resistance: an essential prerequisite for tumor metastasis Int. J. Cell Biol. 2012 2012 306879