Regulation of O2 consumption by the PI3K and mTOR pathways contributes to tumor hypoxia

Radiotherapy and Oncology

Volumn 111, Issue 1, 2014, Pages 72-80

  Kelly, Catherine J ^a   Hussien, Kamila ^a   Fokas, Emmanouil ^a   Kannan, Pavitra ^a   Shipley, Rebecca J ^b   Ashton, Thomas M ^a   Stratford, Michael ^a   Pearson, Natalie ^c   Muschel, Ruth J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Hypoxia; mTOR; Oxidative metabolism; PI3K; Reoxygenation

Indexed keywords

ADENOSINE TRIPHOSPHATE; AZD 8055; BUPARLISIB; CITRATE SYNTHASE; DACTOLISIB; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; OXYGEN; AMINOPYRIDINE DERIVATIVE; IMIDAZOLE DERIVATIVE; MORPHOLINE DERIVATIVE; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; NVP-BKM120; PROTEIN KINASE INHIBITOR; QUINOLINE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL; CANCER CELL LINE; CELL HYPOXIA; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYPOXEMIA; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; MATHEMATICAL MODEL; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; OXYGENATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN TARGETING; RESPIRATORY CHAIN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR NECROSIS; TUMOR SPHEROID; TUMOR XENOGRAFT; VASCULAR TUMOR; WHOLE CELL; ANIMAL TISSUE; CELL FUNCTION; HYPOXIA; MALIGNANT NEOPLASTIC DISEASE; TUMOR HYPOXIA; VASCULAR REMODELING; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYMOLOGY; HCT116 CELL LINE; METABOLISM; MULTICELLULAR SPHEROID; NEOPLASM; PHYSIOLOGY; TUMOR CELL LINE;

AMINOPYRIDINES; ANIMALS; CELL HYPOXIA; CELL LINE, TUMOR; HCT116 CELLS; HUMANS; IMIDAZOLES; MICE; MORPHOLINES; NEOPLASMS; OXYGEN CONSUMPTION; PHOSPHATIDYLINOSITOL 3-KINASE; PROTEIN KINASE INHIBITORS; QUINOLINES; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; TOR SERINE-THREONINE KINASES;

EID: 84902121858     PISSN: 01678140     EISSN: 18790887     Source Type: Journal    
DOI: 10.1016/j.radonc.2014.02.007     Document Type: Article

References (54)

1. M.D. Abramoff, P.J. Magelhaes, and S.J. Ram Image processing with ImageJ Biophoton Int 11 2004 36 42
2. K.J. Ahn, H.S. Hwang, and J.H. Park et al. Evaluation of the role of hexokinase type II in cellular proliferation and apoptosis using human hepatocellular carcinoma cell lines J Nucl Med 50 2009 1525 1532
3. R. Ansiaux, J. Dewever, V. Grégoire, O. Feron, B.F. Jordan, and B. Gallez Decrease in tumor cell oxygen consumption after treatment with vandetanib (ZACTIMA; ZD6474) and its effect on response to radiotherapy Radiat Res 172 2009 584 591
4. C. Betz, D. Stracka, C. Prescianotto-Baschong, M. Frieden, N. Demaurex, and M.N. Hall MTOR complex 2-AKT signaling at mitochondria-associated endoplasmic reticulum membranes (MAM) regulates mitochondrial physiology Proc Natl Acad Sci U S A 110 2013 12526 12534
5. G.N. Bijur, and R.S. Jope Rapid accumulation of AKT in mitochondria following phosphatidylinositol 3-kinase activation J Neurochem 87 2003 1427 1435
6. E.M. Brey, Z. Lalani, and C. Johnston et al. Automated selection of DAB-labeled tissue for immunohistochemical quantification J Histochem Cytochem 51 2003 575 584
7. C.L. Buller, R.D. Loberg, and M.H. Fan et al. A GSK-3/TSC2/mTOR pathway regulates glucose uptake and GLUT1 glucose transporter expression Am J Physiol Cell Physiol 295 2008 C836 C843
8. L.C. Cantley The phosphoinositide 3-kinase pathway Science 296 2002 1655 1657
9. J. Carlsson, and J.M. Yuhas Liquid-overlay culture of cellular spheroids Recent Results Cancer Res 95 1984 1 23
10. G.J. Cerniglia, N. Pore, and J.H. Tsai et al. Epidermal growth factor receptor inhibition modulates the microenvironment by vascular normalization to improve chemotherapy and radiotherapy efficacy PLoS One 4 2009 e6539
11. C. Chen, N. Pore, A. Behrooz, F. Ismail-Beigi, and A. Maity Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia J Biol Chem 276 2001 9519 9525
12. C. Diepart, O. Karroum, and J. Magat et al. Arsenic trioxide treatment decreases the oxygen consumption rate of tumor cells and radiosensitizes solid tumors Cancer Res 72 2011 482 490
13. R.L. Elstrom, D.E. Bauer, and M. Buzzai et al. AKT stimulates aerobic glycolysis in cancer cells Cancer Res 64 2004 3892 3899
14. E. Fokas, J.H. Im, and S. Hill et al. Dual inhibition of the PI3K/mTOR pathway increases tumor radiosensitivity by normalizing tumor vasculature Cancer Res 72 2012 239 248
15. E. Fokas, M. Yoshimura, and R. Prevo et al. NVP-BEZ235 and NVP-BGT226, dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitors, enhance tumor and endothelial cell radiosensitivity Radiat Oncol 7 2012 48
16. I. Garcia-Cao, M.S. Song, and R.M. Hobbs et al. Systemic elevation of PTEN induces a tumor-suppressive metabolic state Cell 149 2012 49 62
17. J.R. Garlich, P. De, and N. Dey et al. A vascular targeted pan phosphoinositide 3-kinase inhibitor prodrug, SF1126, with antitumor and antiangiogenic activity Cancer Res 68 2008 206 215
18. L.H. Gray, A.D. Conger, M. Ebert, S. Hornsey, and O.C. Scott The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy Br J Radiol 26 1953 1638 1648
19. R.K. Jain Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy Science 307 2005 5
20. G.O. Janssens, S.E. Rademakers, and C.H. Terhaard et al. Accelerated radiotherapy with carbogen and nicotinamide for laryngeal cancer: results of a phase III randomized trial J Clin Oncol 30 2012 1777 1783
21. J.H. Kaanders, J. van der Bussink, and A.J. Kogel ARCON: a novel biology-based approach in radiotherapy Lancet Oncol 12 2002 728 737
22. J.H. Kaanders, L.A. Pop, and H.A. Marres et al. Accelerated radiotherapy with carbogen and nicotinamide (ARCON) for laryngeal cancer Radiother Oncol 48 1998 115 122
23. J.H.A.M. Kaanders, J. Bussinka, and A.J. van der Kogel Clinical studies of hypoxia modification in radiotherapy Semin Radiat Oncol 14 2004 233 240
24. D. Kong, M. Okamura, H. Yoshimi, and T. Yamori Antiangiogenic effect of ZSTK474, a novel phosphatidylinositol 3-kinase inhibitor Eur J Cancer 45 2009 857 865
25. J.E. Kurtz, and I. Ray-Coquard PI3 kinase inhibitors in the clinic: an update Anticancer Res 32 2012 2463 2470
26. C. Li, Y. Li, and L. He et al. PI3K/AKT signaling regulates bioenergetics in immortalized hepatocytes Free Radic Biol Med 60 2013 29 40
27. P.C. Manegold, C. Paringer, and U. Kulka et al. Antiangiogenic therapy with mammalian target of rapamycin inhibitor RAD001 (Everolimus) increases radiosensitivity in solid cancer Clin Cancer Res 14 2008 892 900
28. C. Martel, M. Allouche, and D.D. Esposti et al. Glycogen synthase kinase 3-mediated voltage-dependent anion channel phosphorylation controls outer mitochondrial membrane permeability during lipid accumulation Hepatology 57 2013 93 102
29. B. Mukherjee, N. Tomimatsu, K. Amancherla, C.V. Camacho, N. Pichamoorthy, and S. Burma The dual PI3K/mTOR inhibitor NVP-BEZ235 is a potent inhibitor of ATM- and DNA-PKCs-mediated DNA damage responses Neoplasia 14 2012 34 43
30. R. Nassim, J.J. Mansure, S. Chevalier, F. Cury, and W. Kassouf Combining mTOR inhibition with radiation improves antitumor activity in bladder cancer cells in vitro and in vivo: a novel strategy for treatment PLoS One 8 2013 e65257
31. C.L. Neary, and J.G. Pastorino AKT inhibition promotes hexokinase 2 redistribution and glucose uptake in cancer cells J Cell Physiol 228 2013 1943 1948
32. V. Nogueira, Y.C. Park, C.C. Chen, P.Z. Xu, M.L. Chen, and I. Tonic et al. AKT determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis Cancer Cell 14 2008 458 470
33. M. Nordsmark, M. Overgaard, and J. Overgaard Pretreatment oxygenation predicts radiation response in advanced squamous cell carcinoma of the head and neck Radiother Oncol 41 1996 31 39
34. J. Overgaard Hypoxic radiosensitization: adored and ignored J Clin Oncol 25 2007 4066 4074
35. S. Paglin, N.Y. Lee, and C. Nakar et al. Rapamycin-sensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells Cancer Res 2005 2005 11061 11070
36. N. Pore, Z. Jiang, H.-K. Shu, E.J. Bernhard, G.D. Kao, and A. Maity AKT1 activation can augment hypoxia-inducible factor-1α expression by increasing protein translation through a mammalian target of rapamycin-independent pathway Mol Cancer Res 4 2006 471 479
37. A.R. Pries, T.W. Secomb, P. Gaehtgens, and J.F. Gross Blood flow in microvascular networks. Experiments and simulation Circ Res 67 1990 826 834
38. N. Qayum, R.J. Muschel, and J.H. Im et al. Tumor vascular changes mediated by inhibition of oncogenic signaling Cancer Res 69 2009 6347 6354
39. P. Radhakrishnan, U. Baraneedharan, and S. Veluchamy et al. Inhibition of rapamycin-induced AKT activation elicits differential antitumor response in head and neck cancers Cancer Res 73 2013 1118 1127
40. Y. Samuels, Z. Wang, and A. Bardelli et al. High frequency of mutations of the PIK3CA gene in human cancers Science 304 2004 554
41. Y. Sato Persistent vascular normalization as an alternative goal of anti-angiogenic cancer therapy Cancer Sci 102 2011 1253
42. M. Saunders, and S. Dische Clinical results of hypoxic cell radiosensitisation from hyperbaric oxygen to accelerated radiotherapy, carbogen and nicotinamide Br J Cancer 27 1996 5271 5278
43. C.R. Schnell, F. Stauffer, and P.R. Allegrini et al. Effects of the dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor NVP-BEZ235 on the tumor vasculature: implications for clinical imaging Cancer Res 68 2008 6598 6607
44. G. Konstantinidou, E.A. Bey, A. Rabellino, K. Schuster, M.S. Maira, and A.F. Gazdar et al. Dual phosphoinositide 3-kinase/mammalian target of rapamycin blockade is an effective radiosensitizing strategy for the treatment of non-small cell lung cancer harboring K-RAS mutations Cancer Res 69 2009 7644 7652
45. T.W. Secomb, R. Hsu, E.T. Ong, J.F. Gross, and M.W. Dewhirst Analysis of the effects of oxygen supply and demand on hypoxic fraction in tumors Acta Oncol 34 1995 313 316
46. T.W. Secomb, R. Hsu, E.Y. Park, and M.W. Dewhirst Green's function methods for analysis of oxygen delivery to tissue by microvascular networks Ann Biomed Eng 32 2004 1519 1529
47. K.L. Sheldon, E.N. Maldonado, J.J. Lemasters, T.K. Rostovtseva, and S.M. Bezrukov Phosphorylation of voltage-dependent anion channel by serine/threonine kinases governs its interaction with tubulin PLoS One 6 2011 e25539
48. C. Taha, Z. Liu, J. Jin, H. Al-Hasani, N. Sonenberg, and A. Klip Opposite translational control of GLUT1 and GLUT4 glucose transporter mRNAs in response to insulin. Role of mammalian target of rapamycin, protein kinase b, and phosphatidylinositol 3-kinase in GLUT1 mRNA translation J Biol Chem 274 1999 33085 33091
49. M.G. Vander Heiden, N.S. Chandel, X.X. Li, P.T. Schumacker, M. Colombini, and C.B. Thompson Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival Proc Natl Acad Sci U S A 97 2000 4666 4671
50. P. Vaupel Tumor microenvironmental physiology and its implications for radiation oncology Semin Radiat Oncol 14 2004 198 206
51. M.R. Wieckowski, C. Giorgi, M. Lebiedzinska, J. Duszynski, and P. Pinton Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells Nat Protoc 4 2009 1582 1590
52. H.L. Wieman, J.A. Wofford, and J.C. Rathmell Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/AKT regulation of Glut1 activity and trafficking Mol Biol Cell 18 2007 1437 1446
53. Q. Xue, B. Hopkins, C. Perruzzi, D. Udayakumar, D. Sherris, and L.E. Benjamin Palomid 529, a novel small-molecule drug, is a TORC1/TORC2 inhibitor that reduces tumor growth, tumor angiogenesis, and vascular permeability Cancer Res 68 2008 9551 9557
54. J.Y. Yang, H.Y. Yeh, K. Lin, and P.H. Wang Insulin stimulates AKT translocation to mitochondria: implications on dysregulation of mitochondrial oxidative phosphorylation in diabetic myocardium J Mol Cell Cardiol 46 2009 919 926