Activities of multiple cancer-related pathways are associated with BRAF mutation and predict the resistance to BRAF/MEK inhibitors in melanoma cells

Cell Cycle

Volumn 13, Issue 2, 2014, Pages 208-219

  Liu, Dingxie ^a   Liu, Xuan ^b   Xing, Mingzhao ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

Author keywords

BRAF mutation; BRAF V600E inhibitor; Drug resistance; MEK inhibitor; Melanoma; Oncogenic pathway

Indexed keywords

ALPHA INTERFERON; B RAF KINASE; B RAF KINASE INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MYC PROTEIN; SELUMETINIB; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; VEMURAFENIB; ANTINEOPLASTIC AGENT; BENZIMIDAZOLE DERIVATIVE; BRAF PROTEIN, HUMAN; CYTOKINE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE INHIBITOR;

ALGORITHM; ARTICLE; CANCER RESISTANCE; CARCINOGENESIS; COMPUTER MODEL; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; HYPOXIA; MELANOMA; MELANOMA CELL; MICROARRAY ANALYSIS; MULTIPLE CANCER; SUPPORT VECTOR MACHINE; UPREGULATION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MUTATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BENZIMIDAZOLES; CELL LINE, TUMOR; CYTOKINES; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION PROFILING; HUMANS; MELANOMA; MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION;

EID: 84892595980     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.26971     Document Type: Article

References (53)

1. Lens MB, Dawes M. Global perspectives of contemporary epidemiological trends of cutaneous malignant melanoma. Br J Dermatol 2004; 150: 179-85; PMID:14996086; http://dx.doi.org/10.1111/j.1365-2133.2004.05708.x (Pubitemid 38352453)
2. Bollag G, Tsai J, Zhang J, Zhang C, Ibrahim P, Nolop K, Hirth P. Vemurafenib: the first drug approved for BRAF-mutant cancer. Nat Rev Drug Discov 2012; 11: 873-86; PMID:23060265; http://dx.doi.org/10.1038/nrd3847
3. Sullivan RJ, Flaherty K. MAP kinase signaling and inhibition in melanoma. Oncogene 2013; 32:2373-9; PMID:22945644; http://dx.doi.org/10.1038/onc.2012.345
4. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, et al.; BRIM-3 Study Group. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011; 364:2507-16; PMID:21639808; http://dx.doi.org/10.1056/NEJMoa1103782
5. Fedorenko IV, Paraiso KH, Smalley KS. Acquired and intrinsic BRAF inhibitor resistance in BRAF V600E mutant melanoma. Biochem Pharmacol 2011; 82: 201-9; PMID:21635872; http://dx.doi.org/10.1016/j.bcp.2011.05.015
6. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005; 102: 15545-50; PMID:16199517; http://dx.doi.org/10.1073/pnas.0506580102 (Pubitemid 41528093)
7. Bild AH, Yao G, Chang JT, Wang Q, Potti A, Chasse D, Joshi MB, Harpole D, Lancaster JM, Berchuck A, et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 2006; 439: 353-7; PMID:16273092; http://dx.doi.org/10.1038/nature04296 (Pubitemid 43128862)
8. Gatza ML, Lucas JE, Barry WT, Kim JW, Wang Q, Crawford MD, Datto MB, Kelley M, Mathey-Prevot B, Potti A, et al. A pathway-based classification of human breast cancer. Proc Natl Acad Sci U S A 2010; 107: 6994-9; PMID:20335537; http://dx.doi.org/10.1073/pnas.0912708107
9. Freedman JA, Tyler DS, Nevins JR, Augustine CK. Use of gene expression and pathway signatures to characterize the complexity of human melanoma. Am J Pathol 2011; 178: 2513-22; PMID:21641377; http://dx.doi.org/10.1016/j.ajpath. 2011.02.037
10. Gatza ML, Kung HN, Blackwell KL, Dewhirst MW, Marks JR, Chi JT. Analysis of tumor environmental response and oncogenic pathway activation identifies distinct basal and luminal features in HER2-related breast tumor subtypes. Breast Cancer Res 2011; 13:R62; PMID:21672245; http://dx.doi.org/10.1186/bcr2899
11. West M, Ginsburg GS, Huang AT, Nevins Jr. Embracing the complexity of genomic data for personalized medicine. Genome Res 2006; 16:559-66; PMID:16651662; http://dx.doi.org/10.1101/gr.3851306
12. Johansson P, Pavey S, Hayward N. Confirmation of a BRAF mutation-associated gene expression signature in melanoma. Pigment Cell Res 2007; 20: 216-21; PMID:17516929; http://dx.doi.org/10.1111/j.1600-0749.2007. 00375.x (Pubitemid 46776377)
13. Zhuang D, Mannava S, Grachtchouk V, Tang WH, Patil S, Wawrzyniak JA, Berman AE, Giordano TJ, Prochownik EV, Soengas MS, et al. C-MYC overexpression is required for continuous suppression of oncogene-induced senescence in melanoma cells. Oncogene 2008; 27: 6623-34; PMID:18679422; http://dx.doi.org/10. 1038/onc.2008.258
14. Pützer BM, Steder M, Alla V. Predicting and preventing melanoma invasiveness: advances in clarifying E2F1 function. Expert Rev Anticancer Ther 2010; 10: 1707-20; PMID:21080799; http://dx.doi.org/10.1586/era.10.153
15. Damsky WE, Curley DP, Santhanakrishnan M, Rosenbaum LE, Platt JT, Gould Rothberg BE, Taketo MM, Dankort D, Rimm DL, McMahon M, et al. β-catenin signaling controls metastasis in Brafactivated Pten-deficient melanomas. Cancer Cell 2011; 20: 741-54; PMID:22172720; http://dx.doi.org/10.1016/j.ccr.2011.10. 030
16. Satyamoorthy K, Li G, Vaidya B, Patel D, Herlyn M. Insulin-like growth factor-1 induces survival and growth of biologically early melanoma cells through both the mitogen-activated protein kinase and betacatenin pathways. Cancer Res 2001; 61: 7318-24; PMID:11585772 (Pubitemid 32946531)
17. Li Y, Prives C. Are interactions with p63 and p73 involved in mutant p53 gain of oncogenic function? Oncogene 2007; 26: 2220-5; PMID:17401431; http://dx.doi.org/10.1038/sj.onc.1210311 (Pubitemid 46536648)
18. Davies MA, Samuels Y. Analysis of the genome to personalize therapy for melanoma. Oncogene 2010; 29: 5545-55; PMID:20697348; http://dx.doi.org/10.1038/ onc.2010.323
19. Croce CM. Oncogenes and cancer. N Engl J Med 2008; 358: 502-11; PMID:18234754; http://dx.doi.org/10.1056/NEJMra072367 (Pubitemid 351185806)
20. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007; 8: 118-27; PMID:16632515; http://dx.doi.org/10.1093/biostatistics/kxj037 (Pubitemid 44906106)
21. Chang C, Lin LIBSVM. a library for support vector machines. ACM Transactions on Intelligent Systems and Technology 2011; 2: 1-27; http://dx.doi.org/10.1145/1961189.1961199
22. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, Fagin JA, Marlow LA, Copland JA, Smallridge RC, et al. Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 2008; 93: 4331-41; PMID:18713817; http://dx.doi.org/10. 1210/jc.2008-1102 (Pubitemid 352789529)
23. Liu D, Liu X, Xing M. Epigenetic genes regulated by the BRAFV600E signaling are associated with alterations in the methylation and expression of tumor suppressor genes and patient survival in melanoma. Biochem Biophys Res Commun 2012; 425:45-50; PMID:22820187; http://dx.doi.org/10.1016/j.bbrc.2012.07. 046
24. Ellerhorst JA, Greene VR, Ekmekcioglu S, Warneke CL, Johnson MM, Cooke CP, Wang LE, Prieto VG, Gershenwald JE, Wei Q, et al. Clinical correlates of NRAS and BRAF mutations in primary human melanoma. Clin Cancer Res 2011; 17: 229-35; PMID:20975100; http://dx.doi.org/10.1158/1078-0432.CCR-10-2276
25. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky WE Jr., You MJ, DePinho RA, McMahon M, Bosenberg M. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 2009; 41: 544-52; PMID:19282848; http://dx.doi.org/10.1038/ng.356
26. Hoek KS. DNA microarray analyses of melanoma gene expression: a decade in the mines. Pigment Cell Res 2007; 20: 466-84; PMID:17935490; http://dx.doi.org/10.1111/j.1600-0749.2007.00412.x (Pubitemid 47568833)
27. Kupas V, Weishaupt C, Siepmann D, Kaserer ML, Eickelmann M, Metze D, Luger TA, Beissert S, Loser K. RANK is expressed in metastatic melanoma and highly upregulated on melanoma-initiating cells. J Invest Dermatol 2011; 131: 944-55; PMID:21270824; http://dx.doi.org/10.1038/jid.2010.377
28. Girotti MR, Pedersen M, Sanchez-Laorden B, Viros A, Turajlic S, Niculescu-Duvaz D, Zambon A, Sinclair J, Hayes A, Gore M, et al. Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov 2013; 3: 158-67; PMID:23242808; http://dx.doi.org/10. 1158/2159-8290.CD-12-0386
29. Held MA, Langdon CG, Platt JT, Graham-Steed T, Liu Z, Chakraborty A, Bacchiocchi A, Koo A, Haskins JW, Bosenberg MW, et al. Genotypeselective combination therapies for melanoma identified by high-throughput drug screening. Cancer Discov 2013; 3: 52-67; PMID:23239741; http://dx.doi.org/10.1158/2159- 8290.CD-12-0408
30. Bertazza L, Mocellin S. The dual role of tumor necrosis factor (TNF) in cancer biology. Curr Med Chem 2010; 17: 3337-52; PMID:20712570; http://dx.doi.org/10.2174/092986710793176339
31. Khodarev NN, Roizman B, Weichselbaum RR. Molecular pathways: interferon/stat1 pathway: role in the tumor resistance to genotoxic stress and aggressive growth. Clin Cancer Res 2012; 18: 3015-21; PMID:22615451; http://dx.doi.org/10.1158/1078-0432.CCR-11-3225
32. Wang LC, Okitsu CY, Zandi E. Tumor necrosis factor alpha-dependent drug resistance to purine and pyrimidine analogues in human colon tumor cells mediated through IKK. J Biol Chem 2005; 280: 7634-44; PMID:15611081; http://dx.doi.org/10.1074/jbc.M413384200 (Pubitemid 40349656)
33. Yasuoka Y, Naomoto Y, Yamatsuji T, Takaoka M, Kimura M, Uetsuka H, Matsubara N, Fujiwara T, Gunduz M, Tanaka N, et al. Combination of tumor necrosis factor alpha and interferon alpha induces apoptotic cell death through a c-myc-dependent pathway in p53 mutant H226br non-small-cell lung cancer cell line. Exp Cell Res 2001; 271:214-22; PMID:11716533; http://dx.doi.org/10.1006/ excr.2001.5383 (Pubitemid 33141202)
34. Klefstrom J, Arighi E, Littlewood T, Jäättelä M, Saksela E, Evan GI, Alitalo K. Induction of TNFsensitive cellular phenotype by c-Myc involves p53 and impaired NF-kappaB activation. EMBO J 1997; 16: 7382-92; PMID:9405367; http://dx.doi.org/10.1093/emboj/16.24.7382 (Pubitemid 28010498)
35. Boccellino M, Giuberti G, Quagliuolo L, Marra M, D'Alessandro AM, Fujita H, Giovane A, Abbruzzese A, Caraglia M. Apoptosis induced by interferonalpha and antagonized by EGF is regulated by caspase-3-mediated cleavage of gelsolin in human epidermoid cancer cells. J Cell Physiol 2004; 201:71-83; PMID:15281090; http://dx.doi.org/10.1002/jcp.20058 (Pubitemid 39187046)
36. Yamaoka T, Yan F, Cao H, Hobbs SS, Dise RS, Tong W, Polk DB. Transactivation of EGF receptor and ErbB2 protects intestinal epithelial cells from TNF-induced apoptosis. Proc Natl Acad Sci U S A 2008; 105: 11772-7; PMID:18701712; http://dx.doi.org/10.1073/pnas.0801463105
37. Caraglia M, Leardi A, Corradino S, Ciardiello F, Budillon A, Guarrasi R, Bianco AR, Tagliaferri P. alpha-Interferon potentiates epidermal growth factor receptor-mediated effects on human epidermoid carcinoma KB cells. Int J Cancer 1995; 61:342-7; PMID:7729946; http://dx.doi.org/10.1002/ijc.2910610312
38. Carlberg AL, Moberg KH, Hall DJ. Tumor necrosis factor and gamma-interferon repress transcription from the c-myc P2 promoter by reducing E2F binding activity. Int J Oncol 1999; 15: 121-6; PMID:10375604
39. Harvey WH, Harb OS, Kosak ST, Sheaffer JC, Lowe LR, Heerema NA. Interferon-alpha-2b downregulation of oncogenes H-ras, c-raf-2, c-kit, c-myc, c-myb and c-fos in ESKOL, a hairy cell leukemic line, results in temporal perturbation of signal transduction cascade. Leuk Res 1994; 18: 577-85; PMID:7520517; http://dx.doi.org/10.1016/0145-2126(94)90039-6 (Pubitemid 24249379)
40. Wang Y, Roche O, Xu C, Moriyama EH, Heir P, Chung J, Roos FC, Chen Y, Finak G, Milosevic M, et al. Hypoxia promotes ligand-independent EGF receptor signaling via hypoxia-inducible factor-mediated upregulation of caveolin-1. Proc Natl Acad Sci U S A 2012; 109: 4892-7; PMID:22411794; http://dx.doi.org/10. 1073/pnas.1112129109
41. Terui K, Haga S, Enosawa S, Ohnuma N, Ozaki M. Hypoxia/re-oxygenation- induced, redox-dependent activation of STAT1 (signal transducer and activator of transcription 1) confers resistance to apoptotic cell death via hsp70 induction. Biochem J 2004; 380:203-9; PMID:14984365; http://dx.doi.org/10.1042/ BJ20031891 (Pubitemid 38725745)
42. Yu X, Deng L, Wang D, Li N, Chen X, Cheng X, Yuan J, Gao X, Liao M, Wang M, et al. Mechanism of TNF-α autocrine effects in hypoxic cardiomyocytes: initiated by hypoxia inducible factor 1α, presented by exosomes. J Mol Cell Cardiol 2012; 53:848-57; PMID:23085511; http://dx.doi.org/10.1016/j.yjmcc. 2012.10.002
43. Li Q, Kluz T, Sun H, Costa M. Mechanisms of c-myc degradation by nickel compounds and hypoxia. PLoS One 2009; 4:e8531; PMID:20046830; http://dx.doi.org/10.1371/journal.pone.0008531
44. Gerber SA, Pober JS. IFN-alpha induces transcription of hypoxia-inducible factor-1alpha to inhibit proliferation of human endothelial cells. J Immunol 2008; 181: 1052-62; PMID:18606657
45. Hellwig-Bürgel T, Stiehl DP, Wagner AE, Metzen E, Jelkmann W. Review: hypoxia-inducible factor-1 (HIF-1): a novel transcription factor in immune reactions. J Interferon Cytokine Res 2005; 25:297-310; PMID:15957953; http://dx.doi.org/10.1089/jir.2005.25.297 (Pubitemid 40911381)
46. Johnston PA, Grandis Jr. STAT3 signaling: anticancer strategies and challenges. Mol Interv 2011; 11:18-26; PMID:21441118; http://dx.doi.org/10.1124/ mi.11.1.4
47. Grivennikov SI, Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev 2010; 21:11-9; PMID:20018552; http://dx.doi.org/10.1016/j.cytogfr.2009.11.005
48. Mamlouk S, Wielockx B. Hypoxia-inducible factors as key regulators of tumor inflammation. Int J Cancer 2013; 132: 2721-9; PMID:23055435; http://dx.doi.org/10.1002/ijc.27901
49. Majewski IJ, Bernards R. Taming the dragon: genomic biomarkers to individualize the treatment of cancer. Nat Med 2011; 17: 304-12; PMID:21386834; http://dx.doi.org/10.1038/nm.2311
50. Chiarle R, Voena C, Ambrogio C, Piva R, Inghirami G. The anaplastic lymphoma kinase in the pathogenesis of cancer. Nat Rev Cancer 2008; 8:11-23; PMID:18097461; http://dx.doi.org/10.1038/nrc2291
51. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, Wilson CJ, Lehár J, Kryukov GV, Sonkin D, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012; 483:603-7; PMID:22460905; http://dx.doi.org/10.1038/nature11003
52. Guyon I, Weston J, Barnhill S, Vapnik V. Gene Selection for Cancer Classification using Support Vector Machines. Mach Learn 2002; 46: 389-422; http://dx.doi.org/10.1023/A:1012487302797 (Pubitemid 34129977)
53. Dry JR, Pavey S, Pratilas CA, Harbron C, Runswick S, Hodgson D, Chresta C, McCormack R, Byrne N, Cockerill M, et al. Transcriptional pathway signatures predict MEK addiction and response to selumetinib (AZD6244). Cancer Res 2010; 70: 2264-73; PMID:20215513; http://dx.doi.org/10.1158/0008-5472.CAN-09-1577