Acute tumour response to the MEK1/2 inhibitor selumetinib (AZD6244, ARRY-142886) evaluated by non-invasive diffusion-weighted MRI

British Journal of Cancer

Volumn 109, Issue 6, 2013, Pages 1562-1569

  Beloueche Babari, M ^a   Jamin, Y ^a   Arunan, V ^a   Walker Samuel, S ^a   Revill, M ^b   Smith, P D ^b   Halliday, J ^b   Waterton, J C ^b   Barjat, H ^b   Workman, P ^c   Leach, M O ^a   Robinson, S P ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SELUMETINIB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLON CARCINOMA; CONTROLLED STUDY; DIFFUSION COEFFICIENT; DIFFUSION WEIGHTED IMAGING; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR XENOGRAFT;

ANIMALS; BENZIMIDAZOLES; CELL LINE, TUMOR; COLONIC NEOPLASMS; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MAP KINASE KINASE 1; MAP KINASE KINASE 2; MELANOMA; MICE; MICE, NUDE; MOLECULAR TARGETED THERAPY; PROTEIN KINASE INHIBITORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84884588051     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.456     Document Type: Article

References (48)

1. Adjei AA, Cohen RB, Franklin W, Morris C, Wilson D, Molina JR, Hanson LJ, Gore L, Chow L, Leong S, Maloney L, Gordon G, Simmons H, Marlow A, Litwiler K, Brown S, Poch G, Kane K, Haney J, Eckhardt SG (2008) Phase I pharmacokinetic and pharmacodynamic study of the oral, small-molecule mitogen-activated protein kinase kinase 1/2 inhibitor AZD6244 (ARRY-142886) in patients with advanced cancers. J Clin Oncol 26: 2139-2146.
2. Al-Lazikani B, Banerji U, Workman P (2012) Combinatorial drug therapy for cancer in the post-genomic era. Nat Biotechnol 30: 679-692.
3. Aliu SO, Wilmes LJ, Moasser MM, Hann BC, Li KL, Wang D, Hylton NM (2009) MRI methods for evaluating the effects of tyrosine kinase inhibitor administration used to enhance chemotherapy efficiency in a breast tumor xenograft model. J Magn Reson Imaging 29: 1071-1079.
4. Baker LC, Boult JK, Walker-Samuel S, Chung YL, Jamin Y, Ashcroft M, Robinson SP (2012) The HIF-pathway inhibitor NSC-134754 induces metabolic changes and anti-tumour activity while maintaining vascular function. Br J Cancer 106: 1638-1647.
5. Banerji U, de BJ, Judson I, Kaye S, Workman P (2008) Biomarkers in early clinical trials: The committed and the skeptics. Clin Cancer Res 14: 2512-2514.
6. Beloueche-Babari M, Arunan V, Troy H, te Poele RH, te Fong AC, Jackson LE, Payne GS, Griffiths JR, Judson IR, Workman P, Leach MO, Chung YL (2012) Histone deacetylase inhibition increases levels of choline kinase alpha and phosphocholine facilitating noninvasive imaging in human cancers. Cancer Res 72: 990-1000.
7. Bennouna J, Lang I, Valladares-Ayerbes M, Boer K, Adenis A, Escudero P, Kim TY, Pover GM, Morris CD, Douillard JY (2011) A Phase II, openlabel, randomised study to assess the efficacy and safety of the MEK1/2 inhibitor AZD6244 (ARRY-142886) versus capecitabine monotherapy in patients with colorectal cancer who have failed one or two prior chemotherapeutic regimens. Invest New Drugs 29: 1021-1028.
8. Board RE, Ellison G, Orr MC, Kemsley KR, McWalter G, Blockley LY, Dearden SP, Morris C, Ranson M, Cantarini MV, Dive C, Hughes A (2009) Detection of BRAF mutations in the tumour and serum of patients enrolled in the AZD6244 (ARRY-142886) advanced melanoma phase II study. Br J Cancer 101: 1724-1730.
9. Carden CP, Banerji U, Kaye SB, Workman P, de Bono JS (2009) From darkness to light with biomarkers in early clinical trials of cancer drugs. Clin Pharmacol Ther 85: 131-133.
10. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, Hogg D, Lorigan P, Lebbe C, Jouary T, Schadendorf D, Ribas A, O'Day SJ, Sosman JA, Kirkwood JM, Eggermont AM, Dreno B, Nolop K, Li J, Nelson B, Hou J, Lee RJ, Flaherty KT, McArthur GA (2011) Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 364: 2507-2516.
11. Ciuffreda L, Del Bufalo D, Desideri M, Di Sanza C, Stoppacciaro A, Ricciardi MR, Chiaretti S, Tavolaro S, Benassi B, Bellacosa A, Foa R, Tafuri A, Cognetti F, Anichini A, Zupi G, Milella M (2009) Growth-inhibitory and antiangiogenic activity of the MEK inhibitor PD0325901 in malignant melanoma with or without BRAF mutations. Neoplasia 11: 720-731.
12. Corcoran RB, Settleman J, Engelman JA (2011) Potential therapeutic strategies to overcome acquired resistance to BRAF or MEK inhibitors in BRAF mutant cancers. Oncotarget 2: 336-346.
13. Davies BR, Logie A, McKay JS, Martin P, Steele S, Jenkins R, Cockerill M, Cartlidge S, Smith PD (2007) AZD6244 (ARRY-142886), a potent inhibitor of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase 1/2 kinases: Mechanism of action in vivo, pharmacokinetic/pharmacodynamic relationship, and potential for combination in preclinical models. Mol Cancer Ther 6: 2209-2219.
14. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks N, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JWC, Leung SY, Yuen ST, Weber BL, Siegler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR, Futreal PA (2002) Mutations of the BRAF gene in human cancer. Nature 417: 949-954.
15. Dzik-Jurasz A, Domenig C, George M, Wolber J, Padhani A, Brown G, Doran S (2002) Diffusion MRI for prediction of response of rectal cancer to chemoradiation. Lancet 360: 307-308.
16. Englaro W, Bertolotto C, Busca R, Brunet A, Pages G, Ortonne JP, Ballotti R (1998) Inhibition of the mitogen-activated protein kinase pathway triggers B16 melanoma cell differentiation. J Biol Chem 273: 9966-9970.
17. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, O'Dwyer PJ, Lee RJ, Grippo JF, Nolop K, Chapman PB (2010) Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 363: 809-819.
18. Flaherty KT, Robert C, Hersey P, Nathan P, Garbe C, Milhem M, Demidov LV, Hassel JC, Rutkowski P, Mohr P, Dummer R, Trefzer U, Larkin JM, Utikal J, Dreno B, Nyakas M, Middleton MR, Becker JC, Casey M, Sherman LJ, Wu FS, Ouellet D, Martin AM, Patel K, Schadendorf D (2012) Improved survival with MEK inhibition in BRAF-mutated melanoma. N Engl J Med 367: 107-114.
19. Gerstner ER, Chen PJ, Wen PY, Jain RK, Batchelor TT, Sorensen G (2010) Infiltrative patterns of glioblastoma spread detected via diffusion MRI after treatment with cediranib. Neuro-oncol 12: 466-472.
20. Hamstra DA, Rehemtulla A, Ross BD (2007) Diffusion magnetic resonance imaging: A biomarker for treatment response in oncology. J Clin Oncol 25: 4104-4109.
21. Jamin Y, Tucker ER, Poon E, Popov S, Vaughan L, Boult JK, Webber H, Hallsworth A, Baker LC, Jones C, Koh DM, Pearson AD, Chesler L, Robinson SP (2013) Evaluation of clinically translatable MR imaging biomarkers of therapeutic response in the TH-MYCN transgenic mouse model of neuroblastoma. Radiology 266: 130-140.
22. Janne PA, Tsang Shaw A, Rodrigues Pereira J, Jeannin G, Vansteenkiste J, Barrios CH, Franke FA, Grinsted L, Smith PD, Zazulina V, Smith IC, Crino L (2012) Phase II double-blind, randomized study of selumetinib (SEL) plus docetaxel (DOC) versus DOC plus placebo as second-line treatment for advanced KRAS mutant non-small cell lung cancer (NSCLC). J Clin Oncol 30(suppl): Abstract 7503.
23. Jordan BF, Runquist M, Raghunand N, Baker A, Williams R, Kirkpatrick L, Powis G, Gillies RJ (2005) Dynamic contrast-enhanced and diffusion MRI show rapid and dramatic changes in tumor microenvironment in response to inhibition of HIF-1alpha using PX-478. Neoplasia 7: 475-485.
24. Karroum O, Mignion L, Kengen J, Karmani L, Leveque P, Danhier P, Magat J, Bol A, Labar D, Gregoire V, Bouzin C, Feron O, Gallez B, Jordan BF (2013) Multimodal imaging of tumor response to sorafenib combined with radiation therapy: Comparison between diffusion-weighted MRI, choline spectroscopy and 18F-FLT PET imaging. Contrast Media Mol Imaging 8: 274-280.
25. Kim H, Morgan DE, Buchsbaum DJ, Zeng H, Grizzle WE, Warram JM, Stockard CR, McNally LR, Long JW, Sellers JC, Forero A, Zinn KR (2008) Early therapy evaluation of combined anti-death receptor 5 antibody and gemcitabine in orthotopic pancreatic tumor xenografts by diffusionweighted magnetic resonance imaging. Cancer Res 68: 8369-8376.
26. Koh DM, Blackledge M, Collins DJ, Padhani AR, Wallace T, Wilton B, Taylor NJ, Stirling JJ, Sinha R, Walicke P, Leach MO, Judson I, Nathan P (2009) Reproducibility and changes in the apparent diffusion coefficients of solid tumours treated with combretastatin A4 phosphate and bevacizumab in a two-centre phase I clinical trial. Eur Radiol 19: 2728-2738.
27. Koh DM, Scurr E, Collins D, Kanber B, Norman A, Leach MO, Husband JE (2007) Predicting response of colorectal hepatic metastasis: Value of pretreatment apparent diffusion coefficients. Am J Roentgenol 188: 1001-1008.
28. Kono M, Dunn IS, Durda PJ, Butera D, Rose LB, Haggerty TJ, Benson EM, Kurnick JT (2006) Role of the mitogen-activated protein kinase signaling pathway in the regulation of human melanocytic antigen expression. Mol Cancer Res 4: 779-792.
29. Lee KC, Hall DE, Hoff BA, Moffat BA, Sharma S, Chenevert TL, Meyer CR, Leopold WR, Johnson TD, Mazurchuk RV, Rehemtulla A, Ross BD (2006) Dynamic imaging of emerging resistance during cancer therapy. Cancer Res 66: 4687-4692.
30. Loveless ME, Lawson D, Collins M, Nadella MV, Reimer C, Huszar D, Halliday J, Waterton JC, Gore JC, Yankeelov TE (2012) Comparisons of the efficacy of a Jak1/2 inhibitor (AZD1480) with a VEGF signaling inhibitor (cediranib) and sham treatments in mouse tumors using DCE-MRI, DW-MRI, and histology. Neoplasia 14: 54-64.
31. McSheehy PM, Weidensteiner C, Cannet C, Ferretti S, Laurent D, Ruetz S, Stumm M, Allegrini PR (2010) Quantified tumor t1 is a generic earlyresponse imaging biomarker for chemotherapy reflecting cell viability. Clin Cancer Res 16: 212-225.
32. Morse DL, Galons JP, Payne CM, Jennings DL, Day S, Xia G, Gillies RJ (2007) MRI-measured water mobility increases in response to chemotherapy via multiple cell-death mechanisms. NMR Biomed 20: 602-614.
33. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, Chen Z, Lee MK, Attar N, Sazegar H, Chodon T, Nelson SF, McArthur G, Sosman JA, Ribas A, Lo RS (2010) Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 468: 973-977.
34. Padhani AR, Liu G, Koh DM, Chenevert TL, Thoeny HC, Takahara T, Dzik-Jurasz A, Ross BD, Van CM, Collins D, Hammoud DA, Rustin GJ, Taouli B, Choyke PL (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: Consensus and recommendations. Neoplasia 11: 102-125.
35. Schraml C, Schwenzer NF, Martirosian P, Bitzer M, Lauer U, Claussen CD, Horger M (2009) Diffusion-weighted MRI of advanced hepatocellular carcinoma during sorafenib treatment: Initial results. Am J Roentgenol 193: W301-W307.
36. Schubbert S, Shannon K, Bollag G (2007) Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 7: 295-308.
37. Sinkus R, Van Beers BE, Vilgrain V, DeSouza N, Waterton JC (2012) Apparent diffusion coefficient from magnetic resonance imaging as a biomarker in oncology drug development. Eur J Cancer 48: 425-431.
38. Solit DB, Garraway LA, Pratilas CA, Sawai A, Getz G, Basso A, Ye Q, Lobo JM, She Y, Osman I, Golub TR, Sebolt-Leopold J, Sellers WR, Rosen N (2006) BRAF mutation predicts sensitivity to MEK inhibition. Nature 439: 358-362.
39. Tang L, Zhang XP, Sun YS, Shen L, Li J, Qi LP, Cui Y (2011) Gastrointestinal stromal tumors treated with imatinib mesylate: Apparent diffusion coefficient in the evaluation of therapy response in patients. Radiology 258: 729-738.
40. Tunariu N, Kaye SB, DeSouza NM (2012) Functional imaging: What evidence is there for its utility in clinical trials of targeted therapies? Br J Cancer 106: 619-628.
41. Walker-Samuel S, Orton M, McPhail LD, Robinson SP (2009) Robust estimation of the apparent diffusion coefficient (ADC) in heterogeneous solid tumors. Magn Reson Med 62: 420-429.
42. Waterton JC, Pylkkanen L (2012) Qualification of imaging biomarkers for oncology drug development. Eur J Cancer 48: 409-415.
43. Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ, Double JA, Everitt J, Farningham DA, Glennie MJ, Kelland LR, Robinson V, Stratford IJ, Tozer GM, Watson S, Wedge SR, Eccles SA (2010) Guidelines for the welfare and use of animals in cancer research. Br J Cancer 102: 1555-1577.
44. Workman P, Aboagye EO, Chung YL, Griffiths JR, Hart R, Leach MO, Maxwell RJ, McSheehy PMJ, Price PM, Zweit J (2006) Minimally invasive pharmacokinetic and pharmacodynamic technologies in hypothesis-testing clinical trials of innovative therapies. J Natl Cancer Inst 98: 580-598.
45. Workman P, Clarke PA (2011) Resisting targeted therapy: Fifty ways to leave your EGFR. Cancer Cell 19: 437-440.
46. Yang H, Higgins B, Kolinsky K, Packman K, Go Z, Iyer R, Kolis S, Zhao S, Lee R, Grippo JF, Schostack K, Simcox ME, Heimbrook D, Bollag G, Su F (2010) RG7204 (PLX4032), a selective BRAFV600E inhibitor, displays potent antitumor activity in preclinical melanoma models. Cancer Res 70: 5518-5527.
47. Yap TA, Sandhu SK, Workman P, de Bono JS (2010) Envisioning the future of early anticancer drug development. Nat Rev Cancer 10: 514-523.
48. Yeh TC, Marsh V, Bernat BA, Ballard J, Colwell H, Evans RJ, Parry J, Smith D, Brandhuber BJ, Gross S, Marlow A, Hurley B, Lyssikatos J, Lee PA, Winkler JD, Koch K, Wallace E (2007) Biological characterization of ARRY-142886 (AZD6244), a potent, highly selective mitogenactivated protein kinase kinase 1/2 inhibitor. Clin Cancer Res 13: 1576-1583.