Glucose metabolism determines resistance of cancer cells to bioenergetic crisis after cytochrome-c release

Molecular Systems Biology

Volumn 7, Issue , 2011, Pages

  Huber, Heinrich J ^a   Dussmann, Heiko ^a   Kilbride, Seán M ^a   Rehm, Markus ^a   Prehn, Jochen H M ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

apoptosis; bioenergetics; cancer; ODE; single cell imaging

Indexed keywords

CASPASE 3; CYTOCHROME C; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ADENOSINE TRIPHOSPHATE; CASP3 PROTEIN, HUMAN; GLUCOSE;

APOPTOSIS; ARTICLE; BIOENERGY; CANCER CELL; CANCER RESISTANCE; CELL HETEROGENEITY; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; CELL LINE; CELL MEMBRANE POTENTIAL; ENERGY METABOLISM; ENZYMOLOGY; HELA CELL; METABOLISM; THEORETICAL MODEL;

ADENOSINE TRIPHOSPHATE; APOPTOSIS; CASPASE 3; CELL LINE; CYTOCHROMES C; ENERGY METABOLISM; GLUCOSE; HELA CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE POTENTIALS; MITOCHONDRIA; MODELS, THEORETICAL;

EID: 79952322476     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2011.2     Document Type: Article

References (63)

1. Albeck JG, Burke JM, Aldridge BB, Zhang M, Lauffenburger DA, Sorger PK (2008) Quantitative analysis of pathways controlling extrinsic apoptosis in single cells. Mol Cell 30: 11-25 (Pubitemid 351470145)
2. Atlante A, Calissano P, Bobba A, Azzariti A, Marra E, Passarella S (2000) Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death. J Biol Chem 275: 37159-37166 (Pubitemid 32002134)
3. Beard DA (2005) A biophysical model of the mitochondrial respiratory system and oxidative phosphorylation. PLoS Comput Biol 1: e36
4. Beard DA, Qian H (2007) Relationship between thermodynamic driving force and one-way fluxes in reversible processes. PLoS One 2: e144
5. Bentele M, Lavrik I, Ulrich M, Stosser S, Heermann DW, Kalthoff H, Krammer PH, Eils R (2004) Mathematical modeling reveals threshold mechanism in CD95-induced apoptosis. J Cell Biol 166: 839-851 (Pubitemid 39249835)
6. Chesney J, Mitchell R, Benigni F, Bacher M, Spiegel L, Al-Abed Y, Han JH, Metz C, Bucala R (1999) An inducible gene product for 6-phosphofructo-2-kinase with an AU-rich instability element: role in tumor cell glycolysis and the Warburg effect. Proc Natl Acad Sci USA 96: 3047-3052 (Pubitemid 29148841)
7. Chinopoulos C, Adam-Vizi V (2009) Mitochondria as ATP consumers in cellular pathology. Biochim Biophys Acta 1802: 221-227
8. Colell A, Ricci JE, Tait S, Milasta S, Maurer U, Bouchier-Hayes L, Fitzgerald P, Guio-Carrion A, Waterhouse NJ, Li CW, Mari B, Barbry P, Newmeyer DD, Beere HM, Green DR (2007) GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell 129: 983-997 (Pubitemid 46813151)
9. Dash RK, Beard DA (2008) Analysis of cardiac mitochondrial Na+-Ca2+ exchanger kinetics with a biophysical model of mitochondrial Ca2+ handling suggests a 3:1 stoichiometry. J Physiol 586: 3267-3285 (Pubitemid 351984705)
10. Deveraux QL, Reed JC (1999) IAP family proteins\suppressors of apoptosis. Genes Dev 13: 239-252
11. Dussmann H, Kogel D, Rehm M, Prehn JH (2003a) Mitochondrial membrane permeabilization and superoxide production during apoptosis. A single-cell analysis. J Biol Chem 278: 12645-12649 (Pubitemid 36800024)
12. Dussmann H, Rehm M, Kogel D, Prehn JH (2003b) Outer mitochondrial membrane permeabilization during apoptosis triggers caspase-independent mitochondrial and caspase-dependent plasma membrane potential depolarization: a single-cell analysis. J Cell Sci 116: 525-536 (Pubitemid 36231292)
13. Dussmann H, Rehm M, Concannon CG, Anguissola S, Wurstle M, Kacmar S, Voller P, Huber HJ, Prehn JH (2010) Single-cell quantification of Bax activation and mathematical modelling suggest pore formation on minimal mitochondrial Bax accumulation. Cell Death Differ 17: 278-290
14. Ebert BL, Firth JD, Ratcliffe PJ (1995) Hypoxia and mitochondrial inhibitors regulate expression of glucose transporter-1 via distinct Cis-acting sequences. J Biol Chem 270: 29083-29089
15. Elstrom RL, Bauer DE, Buzzai M, Karnauskas R, Harris MH, Plas DR, Zhuang H, Cinalli RM, Alavi A, Rudin CM, Thompson CB (2004) Akt stimulates aerobic glycolysis in cancer cells. Cancer Res 64: 3892-3899 (Pubitemid 38697301)
16. Evans FE, Kaplan NO (1977) 31P nuclear magnetic resonance studies of HeLa cells. Proc Natl Acad Sci USA 74: 4909-4913 (Pubitemid 8227034)
17. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, Rudka T, Bartoli D, Polishuck RS, Danial NN, De Strooper B, Scorrano L (2006) OPA1 controls apoptotic cristae remodeling independentlyfrommitochondrial fusion. Cell 126: 177-189
18. Garedew A, Henderson SO, Moncada S (2010) Activated macrophages utilize glycolytic ATP to maintain mitochondrial membrane potential and prevent apoptotic cell death. Cell Death Differ 17: 1540-1550
19. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2: 156-162
20. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305: 626-629 (Pubitemid 39006738)
21. Gutenkunst RN, Waterfall JJ, Casey FP, Brown KS, Myers CR, Sethna JP (2007) Universally sloppy parameter sensitivities in systems biology models. PLoS Comput Biol 3: 1871-1878 (Pubitemid 350043403)
22. Huber HJ, Laussmann MA, Prehn JH, Rehm M (2010) Diffusion is capable of translating anisotropic apoptosis initiation into a homogeneous execution of cell death. BMC Syst Biol 4: 9
23. Huber HJ, Rehm M, Plchut M, Dussmann H, Prehn JH (2007) APOPTO-CELL-a simulation tool and interactive database for analyzing cellular susceptibility to apoptosis. Bioinformatics 23: 648-650 (Pubitemid 46522606)
24. Imamura H, Nhat KP, Togawa H, Saito K, Iino R, Kato-Yamada Y, Nagai T, Noji H (2009) Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc Natl Acad Sci USA 106: 15651-15656
25. Jurgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D, Reed JC (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 95: 4997-5002 (Pubitemid 28208539)
26. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136 (Pubitemid 27097313)
27. Korzeniewski B, Brown GC (1998) Quantification of the relative contribution of parallel pathways to signal transfer: application to cellular energy transduction. Biophys Chem 75: 73-80 (Pubitemid 28454664)
28. Korzeniewski B, Zoladz JA (2003) Training-induced adaptation of oxidative phosphorylation in skeletal muscles. Biochem J 374: 37-40 (Pubitemid 37046926)
29. Kushnareva Y, Murphy AN, Andreyev A (2002) Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem J368: 545-553 (Pubitemid 35454532)
30. Kushnareva YE, Polster BM, Sokolove PM, Kinnally KW, Fiskum G (2001) Mitochondrial precursor signal peptide induces a unique permeability transition and release of cytochrome c from liver and brain mitochondria. Arch Biochem Biophys 386: 251-260 (Pubitemid 32989315)
31. Lavrik IN (2010) Systems biology of apoptosis signaling networks. Curr Opin Biotechnol 21:551-555
32. Lessene G, Czabotar PE, Colman PM (2008) BCL-2 family antagonists for cancer therapy. Nat Rev Drug Discov 7: 989-1000
33. Li N, Brun T, Cnop M, Cunha DA, Eizirik DL, Maechler P (2009) Transient oxidative stress damages mitochondrial machinery inducing persistent beta-cell dysfunction. J Biol Chem 284: 23602-23612
34. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c Cell 86: 147-157 (Pubitemid 26256586)
35. Luetjens CM, Kogel D, Reimertz C, Dussmann H, Renz A, Schulze-Osthoff K, Nieminen AL, Poppe M, Prehn JH (2001) Multiple kinetics of mitochondrial cytochrome c release in drug-induced apoptosis. Mol Pharmacol 60: 1008-1019 (Pubitemid 33027436)
36. Matsuyama S, Llopis J, Deveraux QL, Tsien RY, Reed JC (2000) Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat Cell Biol 2: 318-325
37. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191: 144-148
38. Munoz-Pinedo C, Guio-Carrion A, Goldstein JC, Fitzgerald P, Newmeyer DD, Green DR (2006) Different mitochondrial intermembrane space proteins are released during apoptosis in a manner that is coordinately initiatedbut can vary in duration. Proc Natl Acad Sci USA 103: 11573-11578 (Pubitemid 44182493)
39. Nicholls DG (1974) Hamster brown-adipose-tissue mitochondria. The control of respiration and the proton electrochemical potential gradient by possible physiological effectors of the proton conductance of the inner membrane. Eur J Biochem 49: 573-583
40. Nicholls DG (1977) The effective proton conductance of the inner membrane of mitochondria from brown adipose tissue. Dependency on proton electrochemical potential gradient. Eur J Biochem 77: 349-356 (Pubitemid 8142831)
41. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80: 315-360 (Pubitemid 30060567)
42. Nicholls DG, Ferguson S (1992) Bioenergetics 2, 2nd edn. New York: Academic Press. ISBN-13:978-0125181242
43. Nicholls DG, Ward MW (2000) Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts. Trends Neurosci 23: 166-174 (Pubitemid 30151213)
44. Pfaff E, Heldt HW, Klingenberg M (1969) Adenine nucleotide translocation of mitochondria. Kinetics of the adenine nucleotide exchange. Eur J Biochem 10: 484-493
45. Plas DR, Talapatra S, Edinger AL, Rathmell JC, Thompson CB (2001) Akt and Bcl-xL promote growth factor-independent survival through distinct effects on mitochondrial physiology. J Biol Chem 276: 12041-12048
46. Poppe M, Reimertz C, Dussmann H, Krohn AJ, Luetjens CM, Bockelmann D, Nieminen AL, Kogel D, Prehn JH (2001) Dissipation of potassium and proton gradients inhibits mitochondrial hyperpolarization and cytochrome c release during neural apoptosis. J Neurosci 21: 4551-4563 (Pubitemid 32565614)
47. Rego AC, Vesce S, Nicholls DG (2001) The mechanism of mitochondrial membrane potential retention following release of cytochrome c in apoptotic GT1-7 neural cells. Cell Death Differ 8: 995-1003 (Pubitemid 32994650)
48. Rehm M, Dussmann H, Prehn JH (2003) Real-time single cell analysis of Smac/DIABLO release during apoptosis. J Cell Biol 162:1031-1043 (Pubitemid 37174186)
49. Rehm M, Huber HJ, Dussmann H, Prehn JH (2006) Systems analysis of effector caspase activation and its control by X-linked inhibitor of apoptosis protein. EMBO J25: 4338-4349 (Pubitemid 44435231)
50. Ricci JE, Gottlieb RA, Green DR (2003) Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol 160: 65-75 (Pubitemid 36091717)
51. Rodriguez-Enriquez S, Marin-Hernandez A, Gallardo-Perez JC, Moreno-Sanchez R (2009) Kinetics of transport and phosphory-lation of glucose in cancer cells. J Cell Physiol 221: 552-559
52. Rossignol R, Gilkerson R, Aggeler R, Yamagata K, Remington SJ, Capaldi RA (2004) Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res 64: 985-993 (Pubitemid 38176901)
53. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA, Korsmeyer SJ (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2: 55-67 (Pubitemid 34065906)
54. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2,-3,-6,-7,-8, and-10 in a caspase-9-dependent manner. J Cell Biol 144: 281-292 (Pubitemid 29066031)
55. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES (1998) Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell 1: 949-957 (Pubitemid 128379256)
56. Stennicke HR, Renatus M, Meldal M, Salvesen GS (2000) Internally quenched fluorescent peptide substrates disclose the subsite preferences of human caspases 1, 3, 6, 7 and 8. Biochem J 350 (Part 2): 563-568
57. Takanaga H, Chaudhuri B, Frommer WB (2008) GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochim Biophys Acta 1778: 1091-1099
58. Vander Heiden M, Cantley L, Thomson C (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033
59. Ward MW, Rego AC, Frenguelli BG, Nicholls DG (2000) Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J Neurosci 20: 7208-7219
60. Waterhouse NJ, Goldstein JC, von Ahsen O, Schuler M, Newmeyer DD, Green DR (2001) Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process. J Cell Biol 153: 319-328 (Pubitemid 34280218)
61. Wu F, Yang F, Vinnakota KC, Bea1rd DA (2007) Computer modeling of mitochondrial tricarboxylic acid cycle, oxidative phosphorylation, metabolite transport, and electrophysiology J Biol Chem 282: 24525-24537 (Pubitemid 47347524)
62. Zhdanov AV, Ward MW, Prehn JH, Papkovsky DB (2008) Dynamics of intracellular oxygen in PC12 Cells upon stimulation of neurotransmission. J Biol Chem 283: 5650-5661
63. Zou H, Yang R, Hao J, Wang J, Sun C, Fesik SW, Wu JC, Tomaselli KJ, Armstrong RC (2003) Regulation of the Apaf-1/caspase-9 apoptosome by caspase-3 and XIAP. J Biol Chem 278: 8091-8098 (Pubitemid 36800549)