Response of BRAF-mutant melanoma to BRAF inhibition is mediated by a network of transcriptional regulators of glycolysis

Cancer Discovery

Volumn 4, Issue 4, 2014, Pages 423-433

  Parmenter, Tiffany J ^a   Kleinschmidt, Margarete ^a,b   Kinross, Kathryn M ^a,b   Bond, Simon T ^c   Li, Jason ^a,b   Kaadige, Mohan R ^g   Rao, Aparna ^a   Sheppard, Karen E ^a,b   Hugo, Willy ^h   Pupo, Gulietta M ^d   Pearson, Richard B ^a,b   McGee, Sean L ^c   Long, Georgina V ^d,e,f   Scolyer, Richard A ^d,e,f   Rizos, Helen ^d   Lo, Roger S ^h   Cullinane, Carleen ^a,b   Ayer, Donald E ^g   Ribas, Antoni ^h   Johnstone, Ricky W ^a,b   Hicks, Rodney J ^a,b   McArthur, Grant A ^a,b   more..

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

^d WESTMEAD HOSPITAL   (Australia)

^e ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^f UNIVERSITY OF SYDNEY   (Australia)

^g UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; DICHLOROACETIC ACID; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; HEXOKINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; THIOREDOXIN INTERACTING PROTEIN; VEMURAFENIB; 6-ACETYL-8-CYCLOPENTYL-5-METHYL-2-(5-PIPERAZIN-1-YLPYRIDIN-2-YLAMINO)-8H-PYRIDO(2,3-D)PYRIMIDIN-7-ONE; BRAF PROTEIN, HUMAN; INDOLE DERIVATIVE; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; PIPERAZINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRIDINE DERIVATIVE; SULFONAMIDE; TRANSCRIPTION FACTOR;

ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION; GENE MUTATION; GENETIC ANALYSIS; GLYCOLYSIS; GROWTH INHIBITION; HUMAN; HUMAN CELL; IC 50; MELANOMA; PHOSPHORYLATION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; HEK293 CELL LINE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GLYCOLYSIS; HEK293 CELLS; HUMANS; INDOLES; MAP KINASE SIGNALING SYSTEM; MELANOMA; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; PYRIDINES; SULFONAMIDES; TRANSCRIPTION FACTORS;

EID: 84897933246     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-13-0440     Document Type: Article

References (35)

1. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324: 1029-33.
2. Levine AJ, Puzio-Kuter AM. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 2010; 330: 1340-4.
3. Engelman JA, Chen L, Tan X, Crosby K, Guimaraes AR, Upadhyay R, et al. Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers. Nat Med 2008; 14: 1351-6.
4. Kinross KM, Brown DV, Kleinschmidt M, Jackson S, Christensen J, Cullinane C, et al. In vivo activity of combined PI3K/mTOR and MEK inhibition in a Kras(G12D);Pten deletion mouse model of ovarian cancer. Mol Cancer Ther 2011; 10: 1440-9.
5. Rivera VM, Squillace RM, Miller D, Berk L, Wardwell SD, Ning Y, et al. Ridaforolimus (AP23573; MK-8669), a potent mTOR inhibitor, has broad antitumor activity and can be optimally administered using intermittent dosing regimens. Mol Cancer Ther 2011; 10: 1059-71.
6. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. N ature 2002; 417: 9 49-54.
7. Gray-Schopfer VC, da Rocha Dias S, Marais R. The role of B-RAF in melanoma. Cancer Metastasis Rev 2005; 24: 165-83.
8. Yun J, Rago C, Cheong I, Pagliarini R, Angenendt P, Rajagopalan H, et al. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science 2009; 325: 1555-9.
9. Lee MH, Lee SE, Kim DW, Ryu MJ, Kim SJ, Kim YK, et al. Mitochondrial localization and regulation of BRAFV600E in thyroid cancer: a clinically used RAF inhibitor is unable to block the mitochondrial activities of BRAFV600E. J Clin Endocrinol Metab 2011; 96: E19-30.
10. Bollag G, Hirth P, Tsai J, Zhang J, Ibrahim PN, Cho H, et al. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAFmutant melanoma. Nature 2010; 467: 596-9.
11. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012; 367: 1694-703.
12. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010; 363: 809-19.
13. Yang H, Higgins B, Kolinsky K, Packman K, Go Z, Iyer R, et al. RG7204 (PLX4032), a selective BRAFV600E inhibitor, displays potent antitumor activity in preclinical melanoma models. Cancer Res 2010; 70: 5518-27.
14. Hauschild A, Grob JJ, Demidov LV, Jouary T, Gutzmer R, Millward M, et al. Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised controlled trial. Lancet 2012; 380: 358-65.
15. Baudy AR, Dogan T, Flores-Mercado JE, Hoeflich KP, Su F, van Bruggen N, et al. FDG-PET is a good biomarker of both early response and acquired resistance in BRAFV600 mutant melanomas treated with vemurafenib and the MEK inhibitor GDC-0973. EJNMMI Res 2012; 2: 22.
16. Sondergaard JN, Nazarian R, Wang Q, Guo D, Hsueh T, Mok S, et al. Differential sensitivity of melanoma cell lines with BRAFV600E mutation to the specific Raf inhibitor PLX4032. J Transl Med 2010; 8: 39.
17. McArthur GA, Puzanov I, Amaravadi R, Ribas A, Chapman P, Kim KB, et al. Marked, homogeneous, and early [18F]fl uorodeoxyglucosepositron emission tomography responses to vemurafenib in BRAFmutant advanced melanoma. J Clin Oncol 2012; 30: 1628-34.
18. Carlino MS, Saunders CA, Haydu LE, Menzies AM Martin Curtis C Jr, Lebowitz PF, et al. (18)F-labelled fl uorodeoxyglucose-positron emission tomography (FDG-PET) heterogeneity of response is prognostic in dabrafenib treated BRAF mutant metastatic melanoma. Eur J Cancer 2013; 49: 395-402.
19. Papandreou I, Goliasova T, Denko NC. Anticancer drugs that target metabolism: is dichloroacetate the new paradigm? Int J Cancer 2011; 128: 1001-8.
20. Parente P, Coli A, Massi G, Mangoni A, Fabrizi MM, Bigotti G. Immunohistochemical expression of the glucose transporters Glut-1 and Glut-3 in human malignant melanomas and benign melanocytic lesions. J Exp Clin Cancer Res 2008; 27: 34.
21. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P Larkin J, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011; 364: 2507-16.
22. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010; 468: 973-7.
23. Corcoran RB, Rothenberg SM, Hata AN, Faber AC, Piris A, Nazarian RM, et al. TORC1 suppression predicts responsiveness to RAF and MEK inhibition in BRAF-mutant melanoma. Sci Transl Med 2013; 5: 196-98.
24. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, et al. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 2007; 282: 14056-64.
25. Zheng B, Jeong JH, Asara JM, Yuan YY, Granter SR, Chin L, et al. Oncogenic B-RAF negatively regulates the tumor suppressor LKB1 to promote melanoma cell proliferation. Mol Cell 2009; 33: 237-47.
26. Dang CV. MYC on the path to cancer. Cell 2012; 149: 22-35.
27. Marin-Hernandez A, Gallardo-Perez JC, Ralph SJ, Rodriguez-Enriquez S, Moreno-Sanchez R. HIF-1alpha modulates energy metabolism in cancer cells by inducing over-expression of specific glycolytic isoforms. Mini Rev Med Chem 2009; 9: 1084-101.
28. Peterson CW, Ayer DE. An extended Myc network contributes to glucose homeostasis in cancer and diabetes. Front Biosci 2011; 16: 2206-23.
29. Kaplon J, Zheng L, Meissl K, Chaneton B, Selivanov VA MaCkay G, et al. A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence. Nature 2013; 498: 109-12.
30. Vander Heiden MG, Chandel NS, Schumacker PT, Thompson CB. Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol Cell 1999; 3: 159-67.
31. Mills CN, Joshi SS, Niles RM. Expression and function of hypoxia inducible factor-1 alpha in human melanoma under non-hypoxic conditions. Mol Cancer 2009; 8: 104.
32. Tsai WB, Aiba I, Long Y, Lin HK, Feun L, Savaraj N, et al. Activation of Ras/PI3K/ERK pathway induces c-Myc stabilization to upregulate argininosuccinate synthetase, leading to arginine deiminase resistance in melanoma cells. Cancer Res 2012; 72: 2622-33.
33. Haq R, Shoag J, Andreu-Perez P, Yokoyama S, Edelman H, Rowe GC, et al. Oncogenic BRAF regulates oxidative metabolism via PGC1alpha and MITF. Cancer Cell 2013; 23: 302-15.
34. Ikediobi ON, Davies H, Bignell G, Edkins S, Stevens C, O'Meara S et al. Mutation analysis of 24 known cancer genes in the NCI-60 cell line set. Mol Cancer Ther 2006; 5: 2606-12.
35. Stark M, Hayward N. Genome-wide loss of heterozygosity and copy number analysis in melanoma using high-density single-nucleotide polymorphism arrays. Cancer Res 2007; 67: 2632-42.