Histone deacetylase inhibition increases levels of choline kinase α and phosphocholine facilitating noninvasive imaging in human cancers

Cancer Research

Volumn 72, Issue 4, 2012, Pages 990-1000

  Beloueche Babari, Mounia ^a   Arunan, Vaitha ^a   Troy, Helen ^a   Te Poele, Robert H ^c   Te Fong, Anne Christine Wong ^a   Jackson, L Elizabeth ^a   Payne, Geoffrey S ^a   Griffiths, John R ^b   Judson, Ian R ^c   Workman, Paul ^c   Leach, Martin O ^a   Chung, Yuen Li ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BELINOSTAT; BRANCHED CHAIN AMINO ACID; CHOLINE; CHOLINE KINASE; CHOLINE KINASE ALPHA; GLUCOSE; LACTIC ACID; PHOSPHORYLCHOLINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL METABOLISM; CHOLINE WATER RATIO; COLON CARCINOMA; COLON TUMOR; CONTROLLED STUDY; GENE EXPRESSION; GLUCOSE UTILIZATION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; METABOLIC PARAMETERS; MOUSE; NONHUMAN; PHOSPHOMONOESTER TOTAL PHOSPHATE RATIO; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; TUMOR XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CHOLINE KINASE; COLONIC NEOPLASMS; DRUG EVALUATION, PRECLINICAL; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MICE, NUDE; PHOSPHORYLCHOLINE; PROSTATIC NEOPLASMS; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84857222410     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-2688     Document Type: Article

References (41)

1. Marks P, Rifkind RA, Richon VM, Breslow R, Miller T, Kelly WK. Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer 2001;1:194-202. (Pubitemid 33741894)
2. Cress WD, Seto E. Histone deacetylases, transcriptional control, and cancer. J Cell Physiol 2000;184:1-16. (Pubitemid 30349623)
3. Wade PA. Transcriptional control at regulatory checkpoints by histone deacetylases: molecular connections between cancer and chromatin. Hum Mol Genet 2001;10:693-8. (Pubitemid 32331577)
4. Weichert W, Roske A, Gekeler V, Beckers T, Ebert MP, Pross M, et al. Association of patterns of class I histone deacetylase expression with patient prognosis in gastric cancer: a retrospective analysis. Lancet Oncol 2008;9:139-48.
5. Weichert W. HDAC expression and clinical prognosis in human malignancies. Cancer Lett 2009;280:168-76.
6. Lane AA, Chabner BA. Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 2009;27:5459-68.
7. Paris M, Porcelloni M, Binaschi M, Fattori D. Histone deacetylase inhibitors: from bench to clinic. J Med Chem 2008;51:1505-29. (Pubitemid 351438836)
8. Tan J, Cang S, Ma Y, Petrillo RL, Liu D. Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J Hematol Oncol 2010;3:5.
9. de Bono JS, Kristeleit R, Tolcher A, Fong P, Pacey S, Karavasilis V, et al. Phase I pharmacokinetic and pharmacodynamic study of LAQ824, a hydroxamate histone deacetylase inhibitor with a heat shock protein-90 inhibitory profile, in patients with advanced solid tumors. Clin Cancer Res 2008;14:6663-73.
10. Ramalingam SS, Maitland ML, Frankel P, Argiris AE, Koczywas M, Gitlitz B, et al. Carboplatin and paclitaxel in combination with either vorinostat or placebo for first-line therapy of advanced non-small-cell lung cancer. J Clin Oncol 2010;28:56-62.
11. Ma X, Ezzeldin HH, Diasio RB. Histone deacetylase inhibitors: current status and overview of recent clinical trials. Drugs 2009;69:1911-34.
12. Ramalingam SS, Belani CP, Ruel C, Frankel P, Gitlitz B, Koczywas M, et al. Phase II study of belinostat (PXD101), a histone deacetylase inhibitor, for second line therapy of advanced malignant pleural mesothelioma. J Thorac Oncol 2009;4:97-101.
13. Banerji U, de Bono J, Judson I, Kaye S, Workman P. Biomarkers in early clinical trials: the committed and the skeptics. Clin Cancer Res 2008;14:2512-4.
14. Carden CP, Banerji U, Kaye SB, Workman P, de Bono JS. From darkness to light with biomarkers in early clinical trials of cancer drugs. Clin Pharmacol Ther 2009;85:131-3.
15. Yap TA, Sandhu SK, Workman P, de Bono JS. Envisioning the future of early anticancer drug development. Nat Rev Cancer 2010;10:514-23.
16. Workman P, Aboagye EO, Chung YL, Griffiths JR, Hart R, Leach MO, et al. Minimally invasive pharmacokinetic and pharmacodynamic technologies in hypothesis-testing clinical trials of innovative therapies. J Natl Cancer Inst 2006;98:580-98. (Pubitemid 43904842)
17. Beloueche-Babari M, Chung YL, Al-Saffar NM, Falck-Miniotis M, Leach MO. Metabolic assessment of the action of targeted cancer therapeutics using magnetic resonance spectroscopy. Br J Cancer 2010;102:1-7.
18. Deberardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008;7:11-20.
19. Tennant DA, Duran RV, Boulahbel H, Gottlieb E. Metabolic transformation in cancer. Carcinogenesis 2009;30:1269-80.
20. Beloueche-Babari M, Workman P, Leach MO. Exploiting tumor metabolism for non-invasive imaging of the therapeutic activity of molecularly targeted anticancer agents. Cell Cycle 2011;10: 2883-93.
21. Aboagye EO. Phosphatidylcholine metabolic transformation and progression signature as a pharmacodynamic biomarker. Oncotarget 2010;1:163-6.
22. Witney TH, Brindle KM. Imaging tumour cell metabolism using hyperpolarized 13C magnetic resonance spectroscopy. Biochem Soc Trans 2010;38:1220-4.
23. Beloueche-Babari M, Arunan VA, Jackson LE, Perusinghe N, Sharp SY, Workman P, et al. Modulation of melanoma cell phospholipid metabolism in response to heat shock protein 90 inhibition. Oncotarget 2010;1:185-97.
24. Chung YL, Troy H, Banerji U, Jackson LE, Walton MI, Stubbs M, et al. Magnetic resonance spectroscopic pharmacodynamic markers of the heat shock protein 90 inhibitor 17-allylamino,17-demethoxygeldanamycin (17AAG) in human colon cancer models. J Natl Cancer Inst 2003;95:1624-33. (Pubitemid 37455930)
25. Beloueche-Babari M, Peak JC, Jackson LE, Tiet MY, Leach MO, Eccles SA. Changes in choline metabolism as potential biomarkers of phospholipase C{gamma}1 inhibition in human prostate cancer cells. Mol Cancer Ther 2009;8:1305-11.
26. Beloueche-Babari M, Jackson LE, Al-Saffar NM, Workman P, Leach MO, Ronen SM. Magnetic resonance spectroscopy monitoring of mitogen-activated protein kinase signaling inhibition. Cancer Res 2005;65:3356-63. (Pubitemid 40524620)
27. Beloueche-Babari M, Jackson LE, Al-Saffar NM, Eccles SA, Raynaud FI, Workman P, et al. Identification of magnetic resonance detectable metabolic changes associated with inhibition of phosphoinositide 3- kinase signaling in human breast cancer cells. Mol Cancer Ther 2006;5:187-96.
28. Al-Saffar NM, Jackson LE, Raynaud FI, Clarke PA, Ramirez de MA, Lacal JC, et al. The phosphoinositide 3-kinase inhibitor PI-103 downregulates choline kinase alpha leading to phosphocholine and total choline decrease detected by magnetic resonance spectroscopy. Cancer Res 2010;70:5507-17.
29. Chung YL, Troy H, Kristeleit R, Aherne W, Jackson LE, Atadja P, et al. Noninvasive magnetic resonance spectroscopic pharmacodynamic markers of a novel histone deacetylase inhibitor, LAQ824, in human colon carcinoma cells and xenografts. Neoplasia 2008;10:303-13. (Pubitemid 351483570)
30. Sankaranarayanapillai M, Tong WP, Maxwell DS, Pal A, Pang J, Bornmann WG, et al. Detection of histone deacetylase inhibition by noninvasive magnetic resonance spectroscopy. Mol Cancer Ther 2006;5:1325-34. (Pubitemid 43881326)
31. Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ, et al. Guidelines for the welfare and use of animals in cancer research. Br J Cancer 2010;102:1555-77.
32. Workman P, Collins I. Probing the probes: fitness factors for small molecule tools. Chem Biol 2010;17:561-77.
33. Wardell SE, Ilkayeva OR, Wieman HL, Frigo DE, Rathmell JC, Newgard CB, et al. Glucose metabolism as a target of histone deacetylase inhibitors. Mol Endocrinol 2009;23:388-401.
34. Poptani H, Bansal N, Jenkins WT, Blessington D, Mancuso A, Nelson DS, et al. Cyclophosphamide treatment modifies tumor oxygenation and glycolytic rates of RIF-1 tumors: 13C magnetic resonance spectroscopy, Eppendorf electrode, and redox scanning. Cancer Res 2003;63:8813-20. (Pubitemid 38064060)
35. Podo F. Tumour phospholipid metabolism. NMR Biomed 1999; 12:413-39. (Pubitemid 30016999)
36. Katz-Brull R, Margalit R, Bendel P, Degani H. Choline metabolism in breast cancer; 2H-, 13C- and 31P-NMR studies of cells and tumors. MAGMA 1998;6:44-52. (Pubitemid 28500268)
37. Banchio C, Lingrell S, Vance DE. Role of histone deacetylase in the expression of CTP:phosphocholine cytidylyltransferase alpha. J Biol Chem 2006;281:10010-5. (Pubitemid 43864534)
38. Glunde K, Jie C, Bhujwalla ZM. Molecular causes of the aberrant choline phospholipid metabolism in breast cancer. Cancer Res 2004;64:4270-6. (Pubitemid 38802433)
39. Ramirez De Molina A, Penalva V, Lucas L, Lacal JC. Regulation of choline kinase activity by Ras proteins involves Ral-GDS and P13K. Oncogene 2002;21:937-46. (Pubitemid 34146307)
40. Ramirez de Molina A, Sarmentero-Estrada J, Belda-Iniesta C, Taron M, Ramirez De Molina V, Cejas P, et al. Expression of choline kinase alpha to predict outcome in patients with early-stage non-small-cell lung cancer: a retrospective study. Lancet Oncol 2007;8:889-97. (Pubitemid 47488053)
41. Qian DZ, Wang X, Kachhap SK, Kato Y, Wei Y, Zhang L, et al. The histone deacetylase inhibitor NVP-LAQ824 inhibits angiogenesis and has a greater antitumor effect in combination with the vascular endothelial growth factor receptor tyrosine kinase inhibitor PTK787/ ZK222584. Cancer Res 2004;64:6626-34. (Pubitemid 39297923)